Cross-Species Affective Neuroscience Decoding of the Primal Affective Experiences of Humans and Related Animals (2011) – PANSKEPP

Introduction

The
most intense affective experiences humans ever have are during
emotional episodes. All other mammals exhibit similar types of emotional
arousals. But do they experience affective states when their external
behaviors are intensely emotional? Most interested scholars and the
public at large answer, “Obviously they do.” This everyday conclusion is
now supported by both behavioral [1] and neuroscientific evidence [2], [3].
However, most careful scholars who scientifically study emotions tend
to assume an agnostic stance. Let me only consider a most recent
example: Mendl, Burman, and Paul [4],
at the beginning of a fine recent paper on the emotional choices made
by animals, carefully indicated that the emotional behaviors of animals
“may or may not be experienced consciously.” An accompanying commentary
on that article highlighted epistemological ways out of such conundrums,
by basing arguments on triangulated evidence from affective
neuroscience [5]—relating
i) brain mechanisms, to both ii) behavior and iii)
experiential-affective analyses (see below). Behavior-only research
cannot achieve definitive conclusions, since it has no direct access to
underlying affective infrastructure of certain brain mechanisms. Thus,
if we just analyze behavior, we have no empirical way out of the
conundrum of belief-based conclusions. With the inclusion of
neuroscience, especially direct evaluation of the affective properties
of the underlying brain systems, we can base our conclusions on
evidence, and the position advanced here is that abundant data has long
indicated that animals do experience their emotional arousals. In short,
activation of various brain systems can serve as “rewards” and
“punishments” in various learning tasks [2].
Thus, we know approximately where affective states are generated in the
brain although we do not know exactly how. Such subcortical loci of
control allow us to entertain the idea that a study of emotional
circuits in animal brains can illuminate the primal sources of human
emotional feelings. But the relevant brain and behavioral/psychological
sciences have yet to embrace such conclusions, and agnosticism prevails.
Thus, this paper is premised on the fact that it is within the brain
mechanisms of unconditioned emotional behaviors where we find the
strongest empirical evidence for the emotional feelings of animals.

Empirical
resolution of the perennial dilemma of subjectively experienced
emotions in other creatures (a form of phenomenal consciousness) raises
important issues for animal welfare debates and provides scientific
paths for working out the neural mechanisms that generate valuative
internal experiences in other animals. That knowledge could guide
understanding of the foundations of our own brains and minds. Of course,
there continues to exist a widespread fear of anthropomorphism in the
cross-species brain sciences (Figure 1), which may no longer be as wise as it seemed just a few decades ago [2].
This paper discusses the kinds of evidence that currently provide the
most robust scientific support for the existence of subjective affective
experiences in the animals we study. Namely, if artificial experimental
arousal of brain networks that control emotional behaviors can also
routinely serve as ‘rewards’ and ‘punishments’ that can guide learning,
then the evidence for certain types of positive and negative experiences
in their brains, may we say minds, is close to
definitive. That is, unless one could routinely demonstrate that
‘rewards’ and ‘punishments’ in humans are typically unconscious—a data
base that does not exist. Thus, the goal of this essay is to discuss
whether other animals are feeling creatures not just on the basis of
reasoned arguments (which is common, see the Denouement at the very end
of this paper), but also in the context of the most relevant
neuroscientific evidence. Thus, the following conclusion is empirically
justified: At the very least, all other mammals experience their
emotional arousals.

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Figure 1. A truth diagram of anthropomorphism.

A
truth diagram relating how we need to think about the possible
affective nature of animals (The true nature of the world) and our
corresponding scientific judgments about the world. Most of the 20th
century was spent believing that the right lower corner was the correct
place to be philosophically so one could avoid Type I errors, namely
concluding something that is not true to be scientifically correct. This
led to discussions of “anxiety-like” behaviors in animals as opposed to
fear in animals. This article is premised on the data-based conclusion
that individuals who are conversant with the relevant data are wise to
situate themselves in the upper left quadrant, since that way we can
avoid Type II errors, namely the failure to detect a real phenomenon,
because we have false beliefs, or inadequate methods to evaluate the
presence of a phenomenon.

doi:10.1371/journal.pone.0021236.g001

Analysis

The Affective Sources of the BrainMind: Cross-Species Neuroevolutionary Perspectives

The behavioral data for animal emotions have been definitive for a long time, from Darwin (1872) to Mendl et al this past year [4],
so to speak. However an equally important but comparatively neglected
issue is whether animals have the kinds of brains that can engender
subjectively experienced states. Such “mind stuff” can only be
scientifically penetrated with functional neuroscience. To reiterate the
most critical point already noted: If one can demonstrate that brain
networks that participate in generating coherent emotional reactions
also mediate ‘rewarding’ and ‘punishing’ states within the
brain, without employing any external objects such as food and water to
train animals, we would have robust evidence for locating central
processing stations for certain types of affective experiences in
specific brain regions and circuits. Further, if certain underlying
circuit attributes in animals (e.g., neurochemistries) modulate the
within-brain processes that lead various external events to be rewarding
and punishing in both animals and humans, we will have fulfilled
another critical experiential prediction. There are abundant
investigations of drug addictions (especially for morphine and various
psychostimulants), that will not be summarized here, that satisfy that
criterion. Further because of evolutionary homologies in the underlying
subcortical brain mechanisms in all mammals, the above knowledge offers
direct predictions to qualitative human experiences following similar
brain manipulations. In other words, if our predictions about changing
internal feelings in humans, derived from the animal data, are supported
by human self-reports, as has often been the case [2], [6], we have additional reasons for confidence that both humans and animals are having similar (albeit not identical) experiences.

Indeed,
the above criteria, based on many studies of electrical stimulation of
the brain (ESB) and chemical stimulation of the brain (CSB), have
supported the existence of emotional feelings in animals for many years;
such stimulation can trigger emotional-behavioral episodes, yielding
brain states of various kinds that also serve to motivate various
learned approach-and-avoidance behaviors, providing abundant evidence
for positive and negative feelings in animals. This gets us as close as
we can presently get scientifically to the mechanisms that
generate affective feelings in mammalian brains. In addition, if humans
report distinct emotional experiences from such brain sites, we have
additional prima facie evidence for corresponding types of
emotional feelings in animals. It could be supposed that the actual
experience of affective states is achieved by higher brain mechanisms
that are activated by emotional arousals, but that would have to be
deemed a “second best” hypothesis for it becomes un-parsimonious by
adding an additional loop of complexity to the overall equation.

Why
has substantive knowledge about animal emotional feelings had so little
effect on the debate about the existence of subjective experiences in
animals? Especially when such knowledge may clarify the sources of
affective emotional experiences in humans? This appears to be due to a
sustained bias during most of the 20^th century that the internal experiences of animals are outside the realm of rigorous scientific inquiry [7].
Of course, the attitude of skepticism is deeply valued by many
scientists, including myself. However, there are many historical
antecedents where, because of this precious attitude, critical lines of
existing evidence were devalued without counter-evidence and hence new
evidence-based conclusions were not adequately considered, and hence
have been long neglected. This has often slowed down the progress of
science because of prevailing biases against transformational concepts
that are unwelcome in the Zeitgeist. For instance, one common bias among
behaviorists of the 20^th century was that the brain did not
need to be understood to have a coherent science of behavior. That
attitude may have seemed fair enough before modern neuroscience, but
because the study of the “black-box” was long marginalized, when
neuroscientific knowledge suggested that an understanding of emotional
states was ripe for the picking, there were few to harvest the low
hanging fruit.

Now
that there is abundant relevant neuroscience in the field (aka,
behavioral neuroscience), which has quite consistently provided evidence
for the rewarding and punishing nature of brain circuits that mediate
emotional behaviors [2], [3], [6],
affective constructs are still not widely used because of the
continuing fear of anthropomorphism, making it a still prevailing
attitude that presently is evolutionarily unfounded (see Figure 1).
The failure of affective concepts to become common currency in animal
research has, I would argue, had negative influence on
cross-disciplinary integrations, which could have rapidly advanced
fields like biological psychiatry, through the recognition that
emotional feelings were ancient functions of medially situated brainstem
regions. Instead, when cognitive neuroscientists became intensely
interested in emotions with the ready availability of modern brain
imaging in the mid 1990s, most investigators accepted the traditional
view that not only was the neocortex the seat of conscious thought, but
also of emotional feelings. As a result, emotional feelings were not
granted to animals, for they were commonly deemed to be a form of
thought, and affective and cognitive processes were envisioned to be
completely interpenetrant in higher brain regions that generated certain
higher cognitive processes such as frontal cortical regions.

Indeed
considering the evolutionarily layered nature of brain organization, I
will argue that one can readily use cross-species anthropomorphic
reasoning at primary-process subcortical MindBrain levels, albeit not at the tertiary-process neocortical levels, as summarized in Figure 2.
These primal evolutionary concepts will be discussed more extensively
after a thumbnail sketch of the recent history of the field that has
generally slowed the acceptance of animal emotional feelings, as a
gateway to understanding both human and animal emotions, as a key topic
of experimental inquiry.

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Figure 2. Levels of control in brain emotion-affective processing.

A
summary of the global levels of control within the brain 1) with 3
general types of affects (red), 2) three types of basic learning
mechanisms (green), and 3) three representative awareness functions
(blue) of the neocortex (which relies completely on multiple levels of
integration, with descending controls down through the basal ganglia to
the thalamus, looping back to neocortex) before it can fully elaborate
both thoughts and behavior).

doi:10.1371/journal.pone.0021236.g002

Historical Perspectives

As
already noted, Charles Darwin (1809–1882), who wrote what is widely
deemed to be the first modern scientific treatment of the subject of
emotions, set the stage by intuiting that animals have emotional lives
not all that different from our own. With his principle of evolutionary
continuity of mind among animals, he suggested that understanding animal
emotions could scientifically illuminate our own emotional lives [8]. Darwin had no problem in imputing emotional feelings to other animals.

Darwin’s
view, however, did not percolate clearly up to the present-day, namely
to the neurobehavioral and neuropsychological sciences. Indeed, the
theories of many subsequent thinkers, starting prominently with William
James, focused on the possibility that higher cognitive regions of the
brain mediate our emotional feelings, not just the many thoughts that
accompany our emotional arousals. Thus, many scholars at present
continue to believe that emotional feelings are a subset of cognitive
processes, as did scholars over a century ago. Indeed, the special whole
issue of Cognition & Emotion devoted to this topic
entitled “How distinctive is affective processing” (published in 2007,
vol 21(6) edited by Andreas Eder, et al.) generally supports the
conclusion that affects are just a subset of cognitive type brain
activities, namely based on sensory information processing principles as
opposed to intrinsic bodily emotional states (i.e., specific forms of
unconditioned responses).

The most famous of these affective-cognitive conflations was advanced in 1885 when William James (1842–1910) [9] and Carl Lange (1834–1900) [10] suggested that emotional feelings merely reflect cortical-cognitive
‘readouts’ of peripheral-unconscious autonomic arousals that occur in
our bodies when we exert ourselves in emergency situations—for instance,
running away from bears. In this interpretation, bodily information
reaches the sensory regions of the cerebral cortex, where the sensations
of bodily arousals are transformed into emotional experiences. In
effect, emotion-related bodily commotions were integrated into emotional
feelings by higher mental processes. Among many scholars, this vision
of emotionality served to bring into question the existence of emotional
feelings in other animals because they have so much less higher
“cognitive brain” matter (i.e., neocortex) compared to humans. But all
this happened before we understood the evolutionary construction of the
brain, and the recognition that many vast emotional integrative
networks, especially for unconditioned emotional responses, were built
into the subcortical structure of all mammalian brains during the long
course of brain evolution.

This
type of neocortical ‘readout’ hypothesis/opinion has survived the test
of time but not the test of experimental evidence—in short, it is still
widely discussed and believed without hardly any critical (causal) evidence to support it, even though brain-imaging correlates can be and often are used to support that archaic conclusion. The
James-Lange theory became ingrained in psychological science belief
systems long before anyone knew much about the emotional networks of
mammalian brains, and there it seems to remain, a well-fossilized
construct. There were compelling challenges as far back as the 1920s [11],
never empirically refuted. Thus, in the emerging brain sciences of the
1970s, the view that we cannot empirically study the emotional feelings
of other animals, because they have relatively little neocortex,
remained the prevailing view, albeit the topic itself was rarely
discussed in neuroscientific circles. Thereby traditional skepticism and
agnosticism continued to prevail as the guiding principles in most rare
discussions of the topic.

Partly,
this stance may have also reflected the widespread rejection of
psychoanalytic theory as a scientific way to conceptualize the mind in
that era. Although Sigmund Freud (1856–1939) had spent the first decade
of his career as a neuroscientist (for a full translation of Freud’s
neuroscientific contributions, see Solms [12]),
his theories, along with those of many of his followers, had made
emotions the centerpiece of his psychoanalytic theories and therapies.
The failure of such ideas to be subjected to rigorous empirical
evaluation, along with the rise of the cognitive and neuroscience
revolutions, also diminished the importance of emotions as a topic for
experimental study because it was deemed too difficult a problem to
solve—namely, how could we ever really know what other animals
experienced?

It
is noteworthy that Freud repeatedly recognized that a lasting
understanding of the mind and emotions, could not be achieved without
neuroscience. He often remarked that we could not make sense of
affective feelings until we came to terms with the inbuilt “instinctual”
nature of emotionality. Freud often claimed that affective states were
never unconscious; they were, by definition, always experienced. But he
recognized that an empirical-neuroscientific understanding of emotions
and other mental-experiential features of the brain could not be
achieved in his era, and he decided not to share his speculative neural
theories, only later discovered in his posthumously published Project for a Scientific Psychology.
But soon thereafter, behavioral scientists definitively denied that it
was empirically possible to study mental events in animals
scientifically, and the book was closed on such topics for a long time.
It is only slowly opening, and usually only with regard to their
self-evident emotional behaviors, as Darwin recognized, but not their
emotional feelings.

As a result, Darwin’s famous dictum [13] that the differences in the mental lives of animals are “one of degree
and not of kind” never served as a jumping-off point for the scientific
understanding of human emotional feelings by studying explicit animal
emotional actions, with but a few exceptions (e.g., MacLean [14] and Panksepp [2]).
The lack of attention paid to the affective lives of other animals, as
opposed to simply their emotional behaviors, by scientists was not
simply because Darwin’s complete view was rather more subtle than the
fragment shared above: “There can be no doubt that the difference
between the mind of the lowest man and that of the highest animal is
immense….Nevertheless the difference….great as it is, certainly is one
of degree and not kind” ([13] p. 127). Now we can be confident that the major degrees of cognitive
differences have arisen from higher brain encephalizations, while
affective feelings are largely sub-neocortical brain functions.

In
sum, the continuing lack of explicit work and discussion in scientific
annals about the neural nature of emotional feelings in animals was
based on the generally accepted ontological view that the subjective
lives of other organisms were impenetrable, while their emotional
behaviors were not. Thus, a cross-species evolutionary approach to
studying the bodies of animals was welcomed, but their minds were neglected. If for no other reason than contextualizing the present
arguments, it is important to be clear about the forces that led
science to neglect the emotional feelings of animals.

So let me flesh out the above history in modest detail. Despite promising initiatives early in the 20^th century, such as the work of Walter Cannon [11] in physiology and McDougall in psychology [15],
discussions of the mental aspects of brain functions that control
animal behaviors withered. With the move toward ultra “positivism” in
philosophy (e.g., the so called Vienna School) which reinforced the
behaviorist revolution, mental concepts in scientific discussions of
animal behaviors seemed less important than ever. Behavior could be
operationalized, but mind could not. The easiest behaviors to study
systematically in the laboratory were those shaped through
‘reinforcement’ contingencies in various automated learning
paradigms—classical conditioning, and training of conditioned lever
presses and such. This led to a radical behaviorism, and B.F. Skinner
(1904–1990) put it bluntly: “The ‘emotions’ are excellent examples of
the fictional causes to which we commonly attribute behavior” [16].
It is no secret that to this day many, perhaps most, behavioral
neuroscientists deny that we have scientific access to the emotional
mind of animals, albeit there are many strands of thinking outside the
scientific mainstream that appreciate the likelihood that animal minds
are real and can be understood (see the final “Denouement” section of
this paper).

Nobel Prize-winning ethologist Niko Tinbergen (1907–1988) put it succinctly and poignantly in his celebrated Study of Instinct (1951) [17]: “Because subjective phenomena cannot be observed objectively in animals, it is idle to claim or deny their existence” ([17] p. 5). In the same period, Nobel laureate Walter Hess discovered that
rage could be readily evoked by ESB of the hypothalamus in cats. Later
in life he indicated that he chose to describe the angry-type attack
behaviors as being ‘sham-rage’ because he did not want to have his work
marginalized by the behaviorist school. In fact, his unshared personal
conviction had been that those rage-like behaviors reflected true
experiences of anger. With the transformation of substantial segments of
methodological behaviorism to “behavioral and cognitive neuroscience”
strategies (starting explicitly in the early 1970s), Hess’s original
views were accepted as state of the art conclusions (despite
demonstrations of the punishing properties of the underlying circuits [2]).
And it is clear to all in the field that discussions of animal
experiences in academic neuroscience and psychology have remained muted
to the present day.

A few ethologists, most prominently Don Griffin (1915–2003) [18], [19], did argue forcefully for cognitive mentality (e.g., thoughts) in animals, and a few others have entertained the existence of experienced emotions in animals (e.g., see the Don Griffin memorial issue of Consciousness & Cognition,
March 2005). However, the upshot of the above history is that, at
present, most scientists seem disinterested or choose to remain agnostic
on such issues. This essay seeks to highlight how abundant
cross-species affective neuroscience research, in fact, now strongly
supports the everyday insight—“of course, other animals have emotional
feelings” without anyone needing to claim that they are identical to the evolutionarily homologous human feelings. Evolution is
diversity, with homologies highlighting relatedness without any claims
about identity.

Thus,
the present essay seeks to bring scientific thinking about these issues
into line with the weight of evidence indicating that all mammals share
not only very similar instinctual emotional behaviors, but that the
activities of the underlying brain networks are closely associated with
the feelings of raw emotion. The implications of these discoveries are
potentially of profound importance for the evolutionary discussions of
human minds, the utility of preclinical translational approaches in
biological psychiatry and the foundational nature of ethics, as well as
the slowly growing appreciation of the evolutionary continuities in
MindBrain functions in all mammals, and probably all other vertebrates.

In
this vision, the primary-process affective mind emerged much earlier in
evolution than our sophisticated cognitive minds. And I will advance
the premise that what came first in evolution, namely that which is
primary-process, still serves as a critical foundation for what came
later, including some of our higher mental abilities. It is likely that
our vast cognitive abilities, and those of other highly cerebrated
mammals, were constructed upon an affective-emotional infrastructure
that all mammals share homologously. Within such a view, many of the
presuppositions of psychology, cognitive science, and neuroscience may
be turned on their collective heads. Many of our higher mental abilities
are comparatively unconscious, meaning unexperienced, for instance, key
aspects of cognitive brain functions such as the basic mechanisms of
learning and memory. In contrast, the affective foundations are
intensely experienced—since they can serve as ‘rewards’ and
‘punishments’ in learning—albeit those psychological states are, at
times, hard to translate into words, symbols which more effectively
describe external sensory-perceptual abilities than emotional ones.

The Evolutionary Layering of the BrainMind

First,
an explanation of the use of the term BrainMind and MindBrain in this
essay: We all know that dualistic thought has traditionally separated
brain and mind, but most neuroscientists who consider such issues now
accept that mental processes, namely internal experiences, are
thoroughly linked to neural dynamics. Hence it may be wiser to have a
monistic term, that does not prioritize either mind or brain, but
combines the concepts into a unified term (common variants are
brain-mind or mind-brain). Perhaps it makes more ontological sense to
simply pull them together into a unified concept, where both variants
can be used flexibly depending on the type of argument pursued: With the
recognition that the brain has retained anatomical signs of
evolutionary layerings, perhaps BrainMind is better for discussing bottom up issues, while MindBrain could be reserved for top-down ones. Since the highest levels of mind
(thoughts and plans) are clearly dependent on neocortical functions,
they are truly much harder to study experimentally and experientially in animals than the basic emotional affects. Implicitly experienced
cognitive processes have no clear behavioral markers as do measures of
affective valence (i.e., rewarding and punishing BrainMind functions
that correspond to certain unconditioned response systems of the brain).

It
has been challenging to generate a coherent nomenclature for
primary-process categories of mind, such as the basic emotions in
animals. I have sought to do this most pointedly for the foundational
level—the primary-process level of analysis that is the focus of this
essay. The primary-process brain mechanisms for emotions are situated
very low and medial in the brain (midbrain, diencephalon and related
basal ganglia) which affirms their ancient nature in brain evolution.
The higher and more forward expansions of the brain provide neural
networks for our higher cognitive abilities. Of course, the layering is
relative, with many integrative issues in-between that bind the
BrainMind into a coherently operating unit.

Still,
if we consider such “layered” evolution of brain organization, as many
neuroscientists do (although perhaps not favored by behaviorists or
cognitivists), then the localization of a variety of emotional circuits
in deep subcortical regions (which unambiguously mediate ‘reward’ and
‘punishment’ functions) strongly supports the conclusion that other
animals do experience their own emotional arousals. The alternative—
that subcortical rewards and punishments are not experienced at all, or
that affective experiences arise only by some type of ‘readout’ by
higher brain mechanisms—is not consistent with the evidence. For
instance, if that were the case, then it would be easier to evoke
rewards and punishments from higher brain regions using brain
stimulation, but as neuroscientists who have conducted such work have
long known, just the reverse is the case. The lower brain systems
sustain reward and punishment functions with the lowest amounts of brain
stimulation. Indeed, there is no coherent stream of data that discrete
activations of neocortical functions in animals arouse any robust reward or punishment functions. In contrast, the existence of unambiguous experimentally evoked subcortical reward and punishment functions, using localized ESB, is vast and
definitive. This provides abundant and consistent support for the idea
that raw affective feelings are, in fact, a property of certain ancient
subcortical midline brain networks in action. However, it does not tell
us exactly what the animal is feeling, only that the feelings
fall in certain categories such as positive and negative affects of
various kinds.

Further,
studies of animals and humans that have been decorticated—i.e., had the
brain’s cortex surgically removed—bear out such conclusions: Primal
emotional responses are spared, even strengthened [20]–[22].
This also fits with the common observation that people with dementia
typically retain emotional responsivity much more than cognitive
abilities. In brief, we have long known that not only can we provoke a
variety of instinctual (unconditioned) emotional patterns in animals
with localized subcortical ESB, but we also know that such evoked states
feel good and bad to animals [3], [6], [23], [24].
It is much harder to be clear about the type of feeling that is
generated. But it is from these same brain zones that we can evoke the
strongest types of diverse self-reports of distinct affective
experiences in humans, and the descriptions of feelings aroused
generally match the emotional behavioral patterns that are evoked in
animals [25], [26]. Further, since we do know that some of the positive effects are discriminated by animals [27] and many can be differentially influenced by direct manipulation of relevant brain chemistries [2],
evidence supports the existence of diverse types of rewarding and
punishing BrainMind states, not just homogenous positive and negative
affective functions.

But is there proof? Scientists, who most value skepticism (i.e., “show me, please”), realize that experimentation never proves anything. It only provides the “weight of evidence” for one view
or another. From that perspective, we should all now agree that various
emotional affective internal experiences have, in fact, been abundantly
and empirically validated in other animals. If not, we would have to
provide evidence and realistic hypothesis-based argumentation for how
environmental ‘rewards’ and ‘punishments’ promote predictable learned
behavioral changes. If they do so without arousing brain affective
processes in animals, we have a conundrum on our hands, since they
routinely have such effects in humans. Thus, at present, skepticism has
gone too far, toward the diametrically opposite realm of belief—that
something already well demonstrated does not, in fact, exist. In other
words, simply saying that certain ‘objects and events’ of the world
‘reinforce’ behavior will not do. “Reinforcement” is not yet a
demonstrated brain function; it is a procedure to train animals. That process in the brain is just a conjecture. The existence of certain affects is not.

It is more coherent, and I would submit, closer to the truth, to say that the concept of reinforcement is the name we give to the way the brain’s primary-process affective
feeling networks facilitate long-term learned behavioral changes.
Indeed, such unconditioned stimulus and response circuits are critical for most of the types of learning commonly studied by behaviorists, to proceed within the brain.

This
could herald a sea change in the way we envision brain mechanisms of
emotional conditioning. Such a view—a modest conceptual
readjustment—could put a very different twist on the underlying
mechanisms that control commonly studied learning such as ‘fear
conditioning’—namely, it may be the raw (unconditional) neural FEAR
integration circuits that generate fearful psychological states that
attract external information into their orbit. In other words the
neuropsychological processes that evolved earlier—e.g., the brain
processes that experimental psychologists traditionally call
“unconditional stimuli” and “unconditional responses”—are of critical
importance for setting up homologous secondary-processes of learning and
memory in all species. Such a levels-of-control vision of evolutionary
BrainMind layering suggests nested-hierarchy types of emotional
organization (Figure 3).

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Figure 3. Nested hierarchies of control within the brain.

A
summary of the hierarchical bottom-up and top-down (circular) causation
that is proposed to operate in every primal emotional system of the
brain. The schematic summarizes the hypothesis that in order for higher
MindBrain functions to mature and function (via bottom-up control), they
have to be integrated with the lower BrainMind functions, with
primary-processes being depicted as squares (red), secondary-process
learning as circles (green), and tertiary processes, by rectangles
(blue). The color-coding aims to convey the manner in which
nested-hierarchies are integrating lower brain functions into higher
brain functions to eventually exert top-down regulatory control (adapted
from Northoff, et al. [47]).

doi:10.1371/journal.pone.0021236.g003

The
primary-process (i.e., basic or primordial) emotions are fine
candidates for such functions. However, they are concentrated in such
deep and ancient neural networks that there are no generally-accepted
experimental strategies to decode their neural nature in humans in any
detail. The subcortical organization of emotional affects in our own
species is now supported by human brain imaging of basic emotions, as
summarized in Figure 4. Animal brain research can achiever higher levels of resolution.

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Figure 4. Overview of brain arousals and inhibitions.

An
overview of brain arousals (reds and yellows) and inhibitions (purples)
depicted on lateral surfaces of the right and left hemispheres (top of
each panel) and medial surfaces of the corresponding hemispheres (bottom
of each panel), while humans experience various basic emotions evoked
by autobiographical reminiscing: Upper left: sadness/GRIEF; upper right:
happiness/JOY; lower left: anger/RAGE; lower right: anxiety/FEAR (data
from Damasio, et al. [38];
overall patterns of activation and inhibition graciously provided by
Antonio Damasio). To highlight the directionality of changes, as
monitored by changes in blood flow, inhibitions are indicated by
downward arrows (predominating in neocortical regions), while arousals
are depicted by upward arrows (predominantly in subcortical regions
where emotional behaviors can be evoked by brain stimulation in
animals).

doi:10.1371/journal.pone.0021236.g004

Without
a solid cross-species neuroscientific foundation, it may be difficult
to make sense of the subsequent mental developments of our species—e.g.,
the way our cognitive apparatus is often subservient to our emotional
feelings. This is inherent in the nested hierarchical view of brain
function depicted in Figure 3.
Thus, at the foundational level, the differences between human
subjective emotional experiences and the mental lives of other mammals
may be “one of degree and not of kind” as Darwin surmised, but now we
know that the subcortical organization of the emotional systems in
mammalian brains is remarkably homologous [2]. An evolutionarily informed cross-species affective neuroscience [3], [23], [24] can now sever the conceptual Gordian knot we have created for ourselves
across the years, and solve the mystery of emotional-affective
experience in humans as well as other animals. But this Darwinian knife
cuts two ways: i) It can return many animals to the ‘circle of affect’
from which they were excluded by scientists, putting additional
responsibilities on scientists who wish to conduct ethical research. ii)
If animals do experience their primary-process emotions and such primal
states of mind serve survival needs, but neuroscientists neglect those
aspects of mammalian BrainMind functions, then there can never be any
deep neuroscientific understanding of the intrinsic values of human
brains. If we continue to neglect the study of emotional experiences in
animals, which is currently still common in the field, we may never
learn how our human affective feelings are generated, and we will
thereby fail to achieve a deep neural understanding of major
evolutionary processes that still control our mind and behavior, and our
various psychiatric disorders.

Synopsis of the Classic Evidence and the Needed Integration With Modern Neuroscience

Arguments
that we will never be able to scientifically measure the emotional
feelings of animals notwithstanding, we have known for a long time that
direct stimulation of a variety of subcortical emotional circuits
generate ‘reward’ and ‘punishment’ functions in various learning tasks
(see research from the era of Delgado, Miller, and colleagues [28], Heath [29] and Olds and Milner [30] in the early 1950s, to the work of MacLean and Panksepp in the 1970s and 80s [14], [23], [31]. There are 21^st century indications of a revival of serious research into the affective functions of mammalian brains [6], [32].

If
the discovery of central nervous system affective ‘rewards’ and
‘punishments’ cannot be used as a reasonable gold standard for
validating the idea that animals do experience their own emotional
arousals, I see no credible experimental approach to understanding
mental states in other animals nor, as a consequence, ever understanding
the neural details of our own raw emotional experiences.

A Terminological Interlude

The
development of a standard scientific nomenclature that can be used to
discuss animal minds, in the present case emotional feelings, is bound
to be a difficult task. Part of the problem is that all our natural
languages are learned skills, tethered to our genetically dictated
communicative urges that are molded into an infinite variety of learned
nuances by our genetically molded articulatory apparatus. And when it
comes to emotional language, there are no rigorous standards that can
easily assure agreement. Just think about the different connotations
that people have for sympathy and empathy, which are
clearly higher-level emotional concepts. The point is, the science of
primary-process animal emotions will surely need a specialized
terminology to minimize confusion. And considering the layers of brain
evolution (symbolized by the upper-left triune-mind logo of Figure 1),
we need distinct labels for primary-process emotions and other affects,
which may be the gateway for understanding higher-order affective
principles. Before proceeding further, let us contemplate the minimal
levels of BrainMind organization that we need to consider (Figure 3).

In
neuroscience, primary-process emotional networks must be defined partly
in terms of empirically delineated neural and behavioral criteria. For
instance, we know that there are subcortical emotional networks that can
generate characteristic emotional-instinctual, behaviorally-evident,
somatically flexible action patterns accompanied by vast
autonomic-visceral changes in the body (i.e., these circuits generate
complex unconditioned responses) that are initially
‘objectless’—they are activated only by a few unconditioned stimuli.
During natural emotional episodes, behavioral and autonomic arousals
outlast the precipitating sensory-perceptual inputs, but this aspect has
not been well-studied using artificial brain stimulations nor
well-controlled studies of natural emotions (i.e., if affective states
are sustained by cognitive ruminations in humans, as they surely are, it
would be harder to evaluate those levels of control in animals). More
speculatively, such emotional arousals that gate/regulate and
selectively process sensory/perceptual inputs into the brain, are
critical controls in the acquisition of learned behaviors that may help
program (and disrupt) many higher brain cognitive/executive functions
(cognitions being defined as elaborations by the brain of
sensory/perceptual inputs from the external world). With emotional
maturation, the developmentally/epigenetically emergent (bottom-up)
higher brain functions come to eventually reciprocally regulate
(top-down) emotional arousals. Obviously, each level adds complexities
to the overall psychobiological equation.

By
definition, emotional affects are subjectively experienced, but this
tells us nothing about how it all happens in the brain. Although the
full emotional package integrates influences from all levels of the
BrainMind (Figures 2 and 3),
it is clear that the primary-processes—the unconditioned emotional
response ssytems—are of critical importance in generating emotional
feelings, but it is not clear that anything at this low level of the
brain deserves the moniker “cognitive”. To the best of our experimental knowledge, primary-process emotional feelings—raw affects—arise
directly from genetically encoded emotional action networks (emotional
‘operating’ systems). For instance when such emotion circuits are
activated in human brains, as by stimulation of the periaqueductal gray
(PAG) of the midbrain, intense feelings are aroused, and they subside
rapidly upon termination [26] presumably because cognitive (secondary- and tertiary-process) factors
are not sustaining the effects. However, such arousals may progressively
lead to endophenotypic shifts in emotional temperaments, as might be
evident in psychiatric disorders.

Overall,
the data are consistent with a dual-aspect monism view of underlying
organization (resembling the dual faces of wave-particle perspectives in
physics)—that raw emotional behaviors and their affects arise from the
same subcortical neural dynamics. These emotional circuits, generating
both emotional behaviors and feelings, anticipate key survival needs,
and there is an evolutionary anticipatory function for both the
behaviors and their primal affective feelings. They tell us promptly
whether a course of action may support survival (namely the various
positive affects) or hinder survival (the negative-aversive feelings).
And in so doing, they mediate what philosophers (e.g., Searle [33]) have called “intentions-in-action” (Figure 2).

But
there are other types of affects than the emotional ones that arise
from the complex dynamics of brain networks. These others are more
closely related to sensory inputs—the pleasures and displeasures of
sensation. And besides the emotional and sensory affects, there are various homeostatic affects of the body—the diverse hungers and thirsts of the body that support somatic health. What they have in common is that they all anticipate events that will help or harm bodily survival. Pain tells us to back
off from certain activities, so as not to injure our bodies any further.
These primal affects are ancestral memories of mammalian brains—built
into the neural infrastructure to promote survival.

This
essay will continue to focus exclusively on those within-brain affects
that are here called “primary-process emotions”—namely, those arising
from complex action-integrating circuits concentrated in subcortical
regions of the brain. In a sense they are most subtle since within-brain
intrinsic precipitants may be as common as external triggers, both by
local tissue irritations (subcortical epileptic foci) as well as higher
cognitive inputs (e.g., ruminations mediated by medial frontal cortical
regions [34], [35]). Thus, this essay summarizes affective neuroscience perspectives on primary-process emotional affects of mammalian brains that seem to unconditionally
arise from the evolutionarily integrated, primordial “instinctual”
emotional operating systems of the brain that regulate unconditioned
emotional actions, which may be more important in guiding simple
emotional learning (e.g., fear-conditioning) than is currently
recognized. This essay also looks at secondary-process emotions
arising from conditioning, both classical and instrumental/operant.
However, with our current scientific tools, we can barely touch the tertiary-process emotion-cognition integrations in animal-models that reflect our
capacity to think and ruminate about our lot in life, which are
concentrated in medial-frontal cortical regions. We are obviously the
most intellectually sophisticated of mammalian species, and thus such
higher neuroaffective issues are best studied in humans, but that is not
to say that the neocortical-cognitive apparatus is able to generate any
affects merely on its own. Its major role is to regulate
emotions—sustaining them with rumination and dampening them with various
regulatory strategies that rely on cortical inhibition of subcortical
processes, what Aristotle called phronesis. Thus, the primordial sources of emotional feelings, important as they are, cannot clarify the whole emotional story.

But
how shall we label the emotional primes (i.e., the distinct
primary-process unconditional emotional response potentials of the
brain)? Holistic MindBrain emotional processes—woven from all
evolutionary levels of mentation—have diverse vernacular terms, such as
anger, loneliness, anxiety, grief, hope, etc., all of which are
tertiary-process concepts. Thus, it would be an error to use such terms
to label the primary-process subcortical emotional-affective functions,
which in my estimation is the most important level for understanding the
evolutionary sources of both animal and human emotion—namely, they are
the fundamental level of brain organization upon which the rest of the
mental apparatus relies [34].
So what terminologies shall we use to discuss that foundational level
so we do not indulge in mereological fallacies—the attribution of the
cause of a holistic body-brain-mind arousal to a part of the body rather
than to the whole?

This
situation mandates a new terminological convention that explicitly
acknowledges levels of control but does not lose touch with the
foundational importance and nature of raw feelings. Thus, here we follow
the terminological choice made a long time ago (full capitalization)
for discussing the primary-process emotions of mammalian minds—namely,
the SEEKING, RAGE, FEAR, LUST, CARE, PANIC/GRIEF and PLAY systems (for a
more complete description of each system, see Appendix S1, with a summarization of key neuroanatomies and neurochemistries in Figure 5).
These labels, by using full-capitalization of terms, refer to specific
subcortical networks in mammalian brains that promote specific
categories of built-in emotional actions and associated feelings. No
claim is made of identity with the corresponding vernacular words,
although profound homologies are anticipated. Although these systems can
never be identical across species (evolutionary diversity rules in all
corners of body and mind), the labeling does seek to acknowledge the
existence of brain networks that govern various class-similar emotional behaviors as well as distinct types of class-similar affective experiences in all mammals. Because of evolutionary
diversification, we may never be able to objectively describe the
precise nature of affective feelings in either humans or animals, but we
can at least have confidence in the existence of meaningful
similarities in the anatomies, neurochemistries, and psychological
functions of these systems across mammalian species. This heuristic will
illuminate the mental lives of animals (Figure 4) as well as provide fundamental knowledge for the development of new and more effective medications of psychiatric problems.

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Figure 5. Overview of key neuroanatomies and neurochemistries of the primary-process emotional networks.

doi:10.1371/journal.pone.0021236.g005

In
sum, primordial emotional feelings are self-evidently highly
interactive with cognitive ‘propositional attitudes’ (each of us feels
strongly about specific emotion-provoking events we encounter
in the world), but such cognitive attitudes are much harder to study
rigorously in animals. Clearly, the cognitive mind of animals is less
experimentally penetrable at a causal neuroscientific level than the
primal affective mind. The above convention for labeling emotional
primes may help us sustain clarity of discussion while minimizing
mereological fallacies, namely part-whole confusions.

Because
the brain is an evolutionarily layered organ, unlike any other in the
body, we must also envision how the various ‘hierarchical’ levels
seamlessly inter-digitate with each other (Figure 3)—in a sense the evolutionary layers of neural networks are completely inter-penetrant (nested-hierarchies) in the intact brain [2], [34].
Thus, key aspects of lower controls are “re-represented” within the
higher levels of control. In this view, during early development the
evolutionarily earlier functions (e.g., the unconditioned aspects)
provide bottom-up control of higher emotional functions. To put it in
other words, lower integrations are functionally embedded in higher
functions that emerged later in the evolution of the brain. In this
manner, earlier/lower brain functions constrain and guide what the more
subtle higher brain functions can achieve, which gradually yield diverse
higher-order emotions that are hard to study in animals, from envy to
shades of jealousy and resentments. Such thoroughly cognitivized
tertiary-processes, thought-related emotions, engendered culturally by
social learning are, at present, next to impossible to study rigorously
at causal levels and most certainly not in animal models.

From a neuroevolutionary perspective, these ‘beehives’ of nested hierarchies allow lower-level controls to maintain some kind of primacy in the overall functionality of higher brain networks, albeit perhaps
not in the immediate control of behavior when the BrainMind has fully
matured. It is likely that the primary processes, upon which
organismic-behavioral coherence is based, continue to anticipate immediate survival issues, which are then passed on to higher levels via learning-conditioning (secondary-processes),
thereby providing information for higher working-memory mechanisms, as
in dorsolateral frontal cortical regions, that permit tertiary-process
deliberative cognitions. Higher forms of consciousness allow humans to
plan farther into the future, based on past experiences, than is
possible for most other animals. Human planning can use memories that go
back toward childhood. This is what is called autonoetic consciousness, in the terminology of Endel Tulving [36],
namely being aware of one’s own life-line from one’s personal
storehouse of memories of the past and hopes for the future. Some
believe that a cross-species affective neuroscience strategy attempts to
marginalize those cortically-mediated cognitive-emotional issues. That
has never been the case. But if we understand the evolution of the
brain, we can more sensitively consider how the higher functional levels
are developmentally/epigenetically constructed.

Such
hierarchically nested schemes may also help us better appreciate
various dilemmas in conceptualizing higher-brain functions and the
participation of such functions in psychiatric disorders (see below).
Scientific study of animals can only inform us well about the operations
of the bottom two levels, with the primary-level being the source of
raw (cognitively-unmodulated) affects, and the many unconscious
mechanisms of secondary-processing (learning & memory) providing
adaptive temporal-spatial patterning of the primary-process affective
potentials which arise from lower layers of the BrainMind. What kind of
additional affective resolution the tertiary-process level may add is
currently unknown, and it is possible that it only mixes the primes
‘neuro-symbolically’ in infinite variations with personal thoughts and
impressions to yield the full complexity of our affective lives,
constructing profound jealousies, demoralizing shame and guilt, abject
desires, and joyous hopes and aspirations—the full human range of
affective life from suffering to serene wisdom (phronesis, as
Aristotle called it; ‘mindfulness’ in modern parlance). This
hierarchical vision may also illuminate why investigators working at
different hierarchical levels rather commonly do not recognize how their
contributions fit into and synergize with different levels of analysis.
This evolutionary scheme allows us to envision how the “construction”
of higher emotional complexities can even emerge via individual
conceptual acts, while not pretending that conceptual acts are the whole
story [37].
When we come to the highest layers of the BrainMind, most developed in
humans, higher emotion-cognition interactions permit humans the
imagination to pursue an almost infinite variety of creative endeavors.
However, those higher brain functions may achieve nothing without the
ancestral affective foundations of our lower minds—the primary affective
processes we share with other mammals.

The Cross-Species Affective Foundations of Emotional Feelings

Without
clear neuroevolutionary approaches, we simply cannot understand the
sources of either human or animal emotional feelings and hence how they
contribute to emotional disorders and to various issues of animal
welfare. In using such cross-species research strategies, we must
explicitly recognize that brains, as evolutionarily layered organs, have
clear imprints of evolutionary progressions within their anatomical and
neurochemical organizations [2], [14], [23].
To summarize, the earliest brain mechanisms remain medially and
caudally situated in brains—in their ancestral locations—with most
recent developments added rostrally and laterally. Functionally, what
emerged earlier remains foundational for later developments, probably
“re-represented” in the nested hierarchies noted earlier (Figure 3). The ancient subcortical locus of human feelings has also been found to be subcortically situated (Figure 4), by Damasio and colleagues [38].

As
we recognize such nested levels of control within the BrainMind, we
should abandon the classic conclusion found in studies on consciousness
that subjective experiences arise only from higher MindBrain regions,
although our “awareness” of such experiences may be so controlled.
Obviously, the lower, phenomenally experienced brain functions (e.g.,
basic emotions and motivations) are more robustly controlled by
inheritance. Higher levels, through social-developmental experiences,
add additional layers of control. Lifetime learning can promote
increasing ‘plasticity’ of psychological strategies and emotional
sentiments that can lead to various moral emotions—from empathy to felt
principles of justice. Such accretions of higher mental functions cannot
be well-studied neuroscientifically, but the other animals also do seem
to have intrinsic moralities [39], as well as capacities to resonate with the distress of others [40].
These moralities are probably expressed in the capacity of animals to
develop perceptually driven affective resonance with others—the
mammalian social principles that allow LUST to become love, for CARE and
PLAY to cement social-support networks and friendships, and PANIC/GRIEF
to provide institutional support structures that allow shared grief to
help heal the psychological pain that might otherwise cascade into
depression.

To
summarize the upshot of this vision: In discussing the neural control
of emotional behaviors and feelings in humans and other animals, we can
usefully parse levels of control into i) primary processes—in
behaviorist parlance, the ‘instinctual’ unconditioned stimuli (UCSs) and
unconditioned responses (UCRs) of the BrainMind; ii) secondary
processes, which reflect the plasticity added by basic mechanisms of
conditioned learning and memory; and iii) in some highly cerebrated
species, tertiary processes (thoughts, deliberations, etc.), allowing
them (and us) to be ‘aware’ of and to reflect upon more primal
experiences. A general principle is that mammals are much more similar
(albeit never identical) in their subcortical network organizations
while being more diversified at higher levels, with the greatest
differences occurring at tertiary-process cortical levels.

Clearly,
the most recent, tertiary-process layers of MindBrain control can only
be well studied in humans. Those higher controls are largely “cognitive”
because they rely heavily on the processing of external information.
Still, both affective and behavioral neuroscience are more effective in
scientifically illuminating the first two levels of control, with
studies of secondary controls being especially well defined by studies
of the brain mechanisms of fear conditioning (e.g., LeDoux [41]; Maren [42]). In contrast, remarkably few have studied the primary-process feelings and neural organizations [6], [43], and how they may actually promote the learning mechanisms of the brain.

It
is important to recognize that the primary-process level is not
‘unconscious’ if one defines consciousness as the ability to have
internal experiences. From the tertiary-process level the
primary-processes may be deemed preconscious, because by itself the
foundational level may not be able to be “aware” of its own
consciousness—those subcortical emotional networks cannot elaborate what
Tulving called noetic (knowing) consciousness. The primal level can only mediate anoetic consciousness—experience without knowing, but intensely experienced
nonetheless. We call this level of experience, affective consciousness [43].

To reiterate, direct ESB-induced activations of these anoetic circuits yield diverse ‘rewards’ and ‘punishments’ that guide learning,
and in humans, we know that the feelings by such brain stimulations are
stronger than those produced by stimulating any other regions of the
brain. The secondary learning processes may be largely unconscious,
simply the parsing of feelings into diverse temporal and spatial
frameworks of individual lives. Tertiary processes are hence mixtures of
raw primal experiences and unconscious learning processes, working
synergistically in working memory, that yield yet other subtleties
(e.g., theories of mind—whereby we are concerned with the thoughts of
others). Tertiary processes also allow the higher brain to develop
networks of social knowledge, as instantiated in mirror neurons—nerve
cells that fire both when an animal/human does something as well as when
another animal/human views that something being done.

However,
there is currently no data indicating that those higher mental
abilities reflect intrinsic brain capacities, as opposed to ones that
emerge via social learning.

In
any event, to understand how the whole BrainMind operates, we must
ultimately consider how higher and lower levels of control participate
in the regulation of the whole [34].
We do not yet have good neuroscientific models for that, except for
human brain imaging along with some more direct measures of neural
activities [44] and, of course, verbal self-reports of experiences. Regardless, all
levels need to be existentially integrated for a balanced life. The main
tools for achieving full integration of levels scientifically might
eventually be through the creative use of massive databases where
genetic, neuroanatomical, neurochemical, and functional information can
be statistically integrated.

The Conundrum of Anoetic Affective Consciousness

There
are no good reasons to think that emotional-feeling mechanisms have
sprung up uniquely in human brains, although some believe it is due to
our great capacity for neocortical working memory [45].
The weight of evidence clearly indicates that many affects arise from
subcortical brain functions that all mammals share. On that score,
cross-species affective neuroscience has already done quite well (e.g.,
Alcaro and colleagues [35], Damasio and coworkers [38], Mobbs and associates [46], Northoff and colleagues [47], [48] and Zubieta and coworkers [49], to name just a few).

Thus,
the real problem is not an epistemological barrier but rather our
failure to deal frankly with the emotional lives of the other animals.
Stated another way, the problem lies more with the history of our field
than with the quantity and quality of the evidence. Indeed, some
prominent investigators who traditionally supposed that higher-brain
functions generate emotional feelings have now tentatively recognized
the critical roles of subcortical loci (e.g., Damasio [50]).

The fact that subjective states cannot be empirically observed as directly as behavior should no longer be seen as an insurmountable dilemma.
Modern neuroscience can probe such hidden functions of the brain using
theoretical strategies that are not all that different conceptually from
those that guided the maturation of quantum physics. Certain processes
in nature (all the way from the mechanisms of gravity to the feelings of
animals) may never be observed directly, and they can only be
probed and illuminated by focusing on objective external signs, indirect
measures, that lead to novel predictions. Measures of emotional
vocalizations may be among the best methods to achieve this in
predictions that go from animals to humans [51]–[56].
To take one example: Rats make two general broad categories of
emotional vocalizations at frequencies that humans can’t hear: i) long
22-kHz-type “complaint” vocalizations when confronted by various
aversive situations, and ii) short 50 kHz-type “chirps” that signal some
kind of positive affect. Clearly those “complaint” networks are
situated in affectively negative brain regions such as the dorsal PAG.
In contrast, when we evoke the positive “chirps” in rats using ESB, at
every brain location where such ‘happy/excited/euphoric’ sounds are
evoked, animals will self-stimulate through those electrodes [52]. Thus, we can infer that those emotional sounds directly monitor the affective states of animals.

Toward a Deeper Psychobiology of the Animal Mind

Epistemological
rigor dictates that those theoretical views that can generate the most
novel predictions and affirmative observations should rule. That is the
time-honored scientific approach to probing the deeper levels of nature
that simply cannot be directly observed. For historical reasons, from
Cartesian dualism to the dogma of radical behaviorism to the
‘computational theory of mind’ computer-driven cognitive revolution [57],
the weight of evidence has not yet had an impact on our discussion of
animal feelings, although empirical support for diverse primary-process
affective feelings within the brains of all mammals has been available
for a long time [2], [3], [6], [58].

That
such evidence has been slow to gain acceptance is not, in fact,
surprising. Among obvious precedents, consider insights from Galileo to
Darwin. A poignant more recent example is the fact that it took the
biological community a decade to accept DNA as the hereditary material,
despite compelling data provided by Oswald Avery (1877–1955) and
colleagues that was published in 1944. The delay arose largely because
most scholars believed that only proteins had the requisite complexity
to mediate something as complex as genetic inheritance.

Currently, perhaps largely because of the pervasive influence of the James-Lange theory of emotions [59], it is still widely believed that emotional feelings reflect the brain’s ability to detect bodily emotional expressions [45],
even though evidence at the primary-process level for such an idea
remains slim (albeit such processes may be present at learned,
secondary-process levels of control [60]).
Many investigators still believe that emotional experiences largely
reflect higher-brain sensory and homeostatic affective functions–such as
those that transpire in frontal, and especially insular, cortices
(e.g., Craig [61]).
And yet there is precious little causal data to believe that those
higher BrainMind levels are the fonts of raw emotional experiences in
neural evolution. Indeed, although there is a mass of data implicating
the insula in the mediation of pain, the quality of taste, and various
somatosensory and interoceptive bodily feelings, this should not be
taken to mean that primal emotional feelings—RAGE, FEAR, PANIC/GRIEF, PLAY etc. (see Appendix S1)
— are constructed there. Although these brain regions routinely “light
up” in imaging of the human brain during various emotional tasks, damage
to these areas typically does not dramatically impair the capacity for
humans to have emotional experiences. As Damasio ([50] p. 77–78) recently noted: “Complete destruction of the insular
cortices, from front to back, in both left and right cerebral
hemispheres, does not result in a complete abolition of feeling. On the
contrary, feelings of pain and pleasure remain. . . Patients report
discomfort with temperature extremes; they are displeased by boring
tasks and are annoyed when their requests are refused. The social
reactivity that depends on the presence of emotional feelings is not
compromised. Attachment is maintained even to persons who cannot be
recognized as loved ones and friends because . . . of concomitant damage
to. . . temporal lobes which severely compromises autobiographical
memory.”

And one can also note that electrical stimulation of those insular regions is not especially robust in evoking strong emotional states of consciousness in humans, although painful sensory-affective feelings are commonly experienced [62].
In contrast, subcortical stimulations evoke coherent emotional
behaviors, including especially strong emotional vocalizations in
animals and strong emotional states in humans [25], [26].
Historical reconstruction of the neuronal connectivities of brain areas
where stereotactic lesions have been used effectively to treat
depressed individuals who have not responded to conventional therapies
highlights the convergence of inputs to primal positive emotional
networks such as the SEEKING system [63].

Results and Discussion

Conclusions

The
issue of whether other animals have internally felt experiences that
contribute to behavioral control has vexed behavioral science since its
inception. Although most investigators remain agnostic on such
contentious issues, there is now abundant experimental evidence
indicating that all mammals have negatively and positively-valenced
emotional networks concentrated in homologous brain regions that may
mediate affective experiences when animals are emotionally aroused. The
relevant lines of evidence are as follows:

1. Brain scientists can evoke powerful emotional responses by localized
   ESB applied to distinct brain regions, similar across all mammalian
   species ever tested. At least 7 types of emotional arousal can be so
   evoked, and we refer to the underlying systems with a special
   nomenclature—SEEKING, RAGE, FEAR, LUST, CARE, PANIC/GRIEF and PLAY.
2. These subcortical structures are homologous among all mammals that
   have been tested. If one arouses the FEAR system, all species studied
   exhibit similar highly negative emotional responses with differences, of
   course, in species-typical details.
3. All of these basic emotional urges, from FEAR to social PLAY, remain
   intact after radical neo-decortication early in life; thus, the
   neocortex is not essential for the generation of primary-process
   emotionality.
4. ESB evoked emotional arousals are not psychologically neutral, since
   all can serve as ‘rewards’ and ‘punishments’ in motivating learning;
   such affective preferences are especially well indexed by conditioned
   place preferences and place aversions as well as by animals’ eagerness
   to turn such ESBs on or off.
5. Comparably localized ESB of human brains yield congruent affective
   experiences—felt emotional arousals that typically appear without
   reason. In concert with the animal data, this provides robust evidence
   for emotional experiences in animals exhibiting primary species-typical
   (instinctual) emotional arousals, and suggests a dual-aspect monism
   strategy whereby instinctual emotional behavior sequences can serve as
   proxies for emotional feelings in animals.

Obviously,
we can only ask if animals experience something by seeing if such
states matter to animals. Will they choose to turn these states on or
off? Will they return to or avoid locations where such states were
artificially evoked (conditioned place preferences and aversions)? If
such intrinsic brain ‘rewards’ and ‘punishments’ are not experienced by other mammals, then we truly have a much bigger puzzle, a
truly profound scientific dilemma, on our hands: How could rewards and
punishments, routinely experienced by humans, control animal behavior
through unconscious neural mechanisms? By simply postulating a spooky
unconscious process called “reinforcement”? In humans, strong emotions
can only be evoked from neural terrain that is demonstrably ancient and
homologous in all mammals. Why would such states evoked from subcortical
regions of human brains be much different from those in animal brains?
Because of neocortical, cognitive ‘readout’ abilities? That is a
supposition that creates more conundrums than it currently solves.

Perhaps
the biggest contribution of cross-species affective neuroscience
research is to decisively return other mammals to their proper status as
conscious, feeling beings. This knowledge can provide new information
about psychiatric disorders, and a fuller understanding of the neural
sources of human affective states (e.g., [64], [65]).
But this knowledge also forces us to face ethical dilemmas. The
implications of such knowledge for how we live with the other creatures
of the world are vast. It is clear that the subcortical powers of our
mind—the diverse affective systems that guide our basic living
patterns—allow us to feel vibrantly alive as well as gloomy despair.
These same systems mediate diverse species typical experiences of ‘rewards’ and ‘punishments’, which may be affectively quite similar across species.

One
implication of this line of research is that we may never understand
the affective depths of our humanity if we ignore our primary-process
emotional continuities with non-human animals. This naturalistic, but
still novel scientific view of animal minds should help clarify the
nature of our own mental lives. If so, it may have enormous implications
for the way we raise our children, treat each other and ourselves, and
how we shall respect the animals with whom we must find better ways to
share the earth.

Denouement

I
write this closing section partly in response to a reviewer of this
article who suggested that I had not been fair about the level of
scientific work that is being pursued on animal emotions these days. As a
point of clarification, I wish to distinguish animal behavior-only and
behavioral neuroscience research on emotions, which is a very vast and
valuable literature, but not one premised on the direct study of
emotional feelings in animals. In contrast, affective neuroscience
strategies seek to lay out causal/constitutive strategies to understand
the underlying ‘mechanisms’ of affective experiences in mammalian
brains. It is noteworthy that primary-process emotions research can be
conducted on fully anesthetized animals, for some indices such as
appetitive sniffing are still expressed under full anesthesia.

In
this essay perhaps I have not conveyed the high level of interest that
exists in the study of emotions outside the realm of neuroscience,
especially among some animal behaviorists. There are abundant articles
on subtle higher-order emotional processes such as empathy, imitation,
and fairness, just to name a few, and certainly there is increasing work
on animal emotional behaviors. Indeed, Marion Dawkins [66] and Franz de Waal [67] have long advocated work on various emotional behaviors of animals, while expressing doubt whether we can make a science out of their emotional states.
If one reads these eminent scholars carefully, it is easy to understand
why they hesitate to talk about or even support talk about emotional experiences,
and implicitly fall back on the agnostic dictum advanced by Nico
Tinbergen: “Because subjective phenomena cannot be observed objectively
in animals, it is idle to claim or deny their existence” (vide supra).

For instance, Dawkins and de Waal have been quite explicit that it is quite impossible to fathom, scientifically, the qualitative experiential nature of animal minds. For instance in her wonderful 1993 book Through Our Eyes Only?, Dawkins questions whether we can experimentally support the contention that animals have true emotional feelings, and
does so in all subsequent writings I have read. For instance in her 2001
discussion of “Who Needs Consciousness?” she ends by saying “it is
important to be clear where observable facts about behavior and
physiology end and assumptions about subjective experiences in other
species begin. However plausible the assumption that other species have
conscious experiences somewhat like ours is, that assumption cannot be
tested in the same way that we can test theories about behavior,
hormones or brain activity” ([66] p. S28). de Waal has done the same, with some softening of that perspective (see end of this “Denouement”).

Their
nuanced points of view miss my point: A causal neuroscientific analysis
has changed the ‘ballgame’. We can now make a variety of testable
predictions about the experiential aspects of artificial arousal of
brain emotional circuits and how such knowledge can impact human
experiences. Now it is no longer a matter of argumentation, but the
“weight of evidence”! And that is all science ever has. At present the
weight of evidence, based on predictions that have been made, is
overwhelmingly for the side of animal affective experiences, with hardly
a feather of support for the other side. Scientists, being ultimate
skeptics, should honor the rules of the science game, and accept that
the neuroscientific evidence now dramatically supports the existence of
diverse affective feelings. Acceptance of the evidence opens up the real
possibility that we can decode the foundations of human emotions
through the study of animal brain functions.

Other scientists working more in the popular vein, especially Marc Bekoff [39],
have had no such hesitations; he suggests that our sympathy for nature,
along with observations of the nuances of animal behaviors, are
sufficient to cross the trans-species mental bridge. I agree as a
person, but not as a scientist, especially since the science now
provides a solid bridge for individuals who have great emotional
sensitivity to other animals to employ scientifically sound arguments
rather than their personal convictions. For instance, I remember sitting
around a campfire with three friends and visiting members of an
elephant conservancy group at the Timbavati Reserve adjoining Kruger
Park in South Africa in the fall of 2008. These protectors of the
elephants were worrying about how many people keep telling them that
other animals, including elephants, do not have emotional feelings, only
humans do. I explained how the scientific data from affective
neuroscience empirically negates those traditional beliefs, and shared
how a strong rebuttal of those ingrained beliefs simply requires the
accurate communication of already existing evidence—data of the type
already discussed here.

My
argument is that sensitive positions that are concurrently liberal at
emotional behavioral levels but conservative at phenomenological
scientific levels, such as those advanced by Dawkins and de Waal, may
still be appropriate for higher-order cognitive aspects of
animal mental lives (e.g., their possible cognitions and thoughts), but
that skepticism should no longer apply to their emotional feelings (affects).
This is simply because the valenced neural infrastructure of affective
states has been well studied with traditional functional neuroscientific
methods [2],
which provide the scientific evidence for the current arguments. Since
this kind of science requires neural investigations, and few animal
behaviorists pursue such work, it is understandable that they have not
fully weighed the many opportunities to go down to the subjective level empirically with the aid of neuroscience. That would not only support their own
views about the importance of emotions in animal lives, but also provide
an epistemology for further progress. Strangely, they have not yet
seized that empirical opportunity, nor recognized the robust
experimental strategies neuroscience provides. As a result, the power of
a very traditional form of skepticism currently continues to outweigh
the evidence even in the minds of the most sensitive investigators of
animal behavior.

This
does not mean that we can read animal minds in any detail, but we can
read the affective arousals and the types of valences that permeate
their minds. When integrated with comparable human research—work that is
routinely happening in the context of neurosurgery for various
disorders (Parkinson’s disease, depression, etc.) with therapeutic deep
brain stimulation—we can also make concrete predictions, and thereby
obtain corroboratory evidence [68] about homologous class-similarities in our affective experiences. The
massive subcortical concentration of affective circuits suggests that
such BrainMind capacities evolved long before the more recent radiations
of mammalian diversity. Species diversity surely means there will be
many differences in the types, durations and intensities of emotional
feelings among different species and different individuals (including
humans), but this does not markedly reduce the possibility of
discovering general principles that work across species.

To
my knowledge neither Dawkins nor de Waal has considered their
“subjectivist dilemma” of other minds, whether in humans or other
animals, and recognized how severely it hinders the acceptance of the
affective neuroscience perspective advocated here. Thus, the empirical
study of emotional feelings has been a workable problem in neuroscience
for some time, although few have “taken the plunge” so to speak. There
are now abundant cross-species neuro-affective predictions that can be
made [2], [65], [68].

On the other hand, various scholars, writing in the popular mode, such as Temple Grandin [1], [63], and most prominently Marc Bekoff [39] accept the reality of animal feelings. But these scholars, and many
others with enlightened views, have not pursued neuroscientific research
on emotional processes. Hence their important advocacies of seemingly
self-evident intuitions are not the same as advancing the rigorous
predictions allowed by neuroscientific approaches. Neuroscience, after
all, is the only way to verify such constructs and also to illuminate
what it means, mechanistically (constitutively), to have subjective
experiences. Hopefully my forceful arguments in behalf of affective
neuroscience strategies, contextualized in hopefully an accurate
portrayal of historical antecedents, will not be envisioned as mere
complaints or empirically unjustified anthropomorphism. The intent is to
advance the science of mind.

We
can finally capitalize on evidence-based neuroevolutionary strategies
to understand other minds, not only to illuminate the affective
mentalities of other creatures, but also to better understand our own.
Why are such endeavors so important? Such knowledge has remarkable
potential to advance the understanding of our own emotional feelings,
scientifically, perhaps for the first time in human history. With this
knowledge we can advance psychiatric insights and aspire to
scientifically respect the minds of other creatures—understanding how
they could feel their emotions as intensely as we do.

Of
course the terms used in consciousness studies—sentience, awareness,
subjectivity, affects, feelings—cannot be precise, and are, no doubt,
used differently by different scholars. For me the simplest and easiest
is the word “experience”—namely certain brain states feel like something
subjectively, and thus deserve to be called phenomenally conscious. Of
course, others may only choose to use the term conscious, when animals
can be shown to be “aware of” (can think and reflect upon) their
experiences. I think that is too biased and shortsighted a view.

If one uses the concept of consciousness phenomenally, anchored simply by the existence of subjective experiences,
it seems likely that primary-process consciousness comes in two major
varieties—cognitive (linked to exteroceptive, perception-generating
sensory inputs) and affective (internal states that feel good and bad in
distinct ways). If so, as we consider the evolutionary layering of the
BrainMind (Figure 2),
we should recognize that affective functions are more medial in the
brain than external perceptual ones, suggesting that affect is more
ancient, and hence would have had priority in the construction of the
mental apparatus. Perhaps the term “awareness” should be reserved just
for higher forms of perceptual consciousness. By my wits, sensory
perceptions, in some currently unknown way, may have arisen from the
pre-existing neural platform for affective neurodynamics [2], [6], [43]. If so, affective experiential states may still be independent of the cognitive knowledge that you are experiencing such brain states.

In
closing, I would note that just as the final revision of this
manuscript was completed, a fine paper on this topic by Franz de Waal
appeared [67] which presents a compelling argument for scientists to develop a
renewed interest in emotions but in ways that “avoid unanswerable
questions and to view emotions as mental and bodily states that
potentiate behavior appropriate to environmental challenges” (p. 191).
In this paper de Waal provides a compelling argument for the importance
of animal emotions, while not crossing the Rubicon to discussions of
emotional experiences.

As
de Waal now expresses, in a toned down way compared to an earlier
version of the manuscript (I was a reviewer), we can study animal
emotions “without knowing much of anything about associated experiences”
(p. 199) and that “the greatest obstacle to the study of animal
emotions is the common objection that “we cannot know what they feel.”
While this is undeniably true, we should realize that such problems also
hold for fellow human beings (p. 199). But affective neuroscience
strategies now provide the needed “weight of evidence” indicating that
animals do “feel” although, admittedly, we cannot be very precise about
the experienced nature of their feelings, above and beyond several
distinct forms of good and bad emotional feelings. But how their brains
allow them to feel good and bad in various ways will, one day, inform us
scientifically, for the first time, about the nature of our own
feelings. The cross-species ethical consequences of this knowledge,
although intuited by many, are huge.

Supporting Information

Appendix S1.

doi:10.1371/journal.pone.0021236.s001

(DOC)