Short-and long-lasting consequences of novelty, deviance and surprise on brain and cognition (2015)

Neuroscience & Biobehavioral Reviews

Available online 11 May 2015

Highlights

  • Stimulus novelty improves perception and facilitates responses.
  • Spatial novelty increases motivation and promotes learning and memory.
  • The effects on perception may be mediated by limbic regions.
  • The effects on responses are short-lived and may be related to LC–NE responses.
  • The effects on learning are longer-lasting and are related to the SN/VTA responses.

Abstract

When one encounters a novel stimulus this sets off a cascade of brain responses, activating several neuromodulatory systems. As a consequence novelty has a wide range of effects on cognition; improving perception and action, increasing motivation, eliciting exploratory behavior, and promoting learning. Here, we review these benefits and how they may arise in the brain. We propose a framework that organizes novelty’s effects on brain and cognition into three groups.

First, novelty can transiently enhance perception. This effect is proposed to be mediated by novel stimuli activating the amygdala and enhancing early sensory processing.

Second, novel stimuli can increase arousal, leading to short-lived effects on action in the first hundreds of milliseconds after presentation. We argue that these effects are related to deviance, rather than to novelty per se, and link them to activation of the locus-coeruleus norepinephrine system.

Third, spatial novelty may trigger the dopaminergic mesolimbic system, promoting dopamine release in the hippocampus, having longer-lasting effects, up to tens of minutes, on motivation, reward processing, and learning and memory.


 

EXCERPTS FROM STUDY

An interest in the new can thus be beneficial, and may also be required to detect potential threats and avert harm. To optimally adapt behavior to the current situation the brain has to make a trade-off between exploiting well-known sources of reward on the one hand, and exploring new objects and situations on the other that may signal more profitable out-comes, or an unknown source of threat.

It has been suggested by computational theories of reinforcement learning that novelty may promote exploratory behavior novelty by eliciting an ‘exploration bonus’ (or novelty bonus), motivating exploratory behavior in search for reward (Düzel et al., 2010; Kakade and Dayan, 2002; Knutson and Cooper, 2006). This idea has been worked out in a theory: NOvelty-related Motivation of Anticipation and exploration by Dopamine or NOMAD (Düzel et al., 2010).NOMAD suggests that perceiving a novel stimulus results in both temporally specific phasic bursts of DA, which increases plasticity both for storage of the novel stimulus itself and of stimuli that follow it, and an increase in tonic DA levels. Moreover, the mere anticipation of novelty would already lead to an increase in tonic DA levels. This increase in tonic activity would in turn enhance reward anticipation and promote exploratory behavior.

Empirical evidence for this theory has shown that novel stimuli and anticipation of novel stimuli can indeed activate the dopa-minergic reward system, enhancing reward prediction responses(Bunzeck et al., 2012; Wittmann et al., 2007), and ensuring that novel opportunities are evaluated and potential risks are assessed until the outcome is known (Krebs et al., 2009). Moreover, nov-elty increases phasic DA release in the striatum to reward (Bunzecket al., 2007; Guitart-Masip et al., 2010; Krebs et al., 2011; Lismanand Grace, 2005). In addition, VTA activity caused by reward anticipation was found to be correlated with better episodic memory, suggesting that DA release can indeed boost memory (Murty and Adcock, 2014). In the other direction, reward can accelerate novelty processing (Bunzeck et al., 2009), a process believed to be controlled by DA, that also modulates memory retrieval performance (Apitz and Bunzeck, 2013; Eckart and Bunzeck, 2013; for a review on the link between dopamine and memory see Shohamy and Adcock, 2010). However, the link between novelty and learning has also been associated with other neuromodulatory systems.

However, the link between novelty and learning has also been associated with other neuromodulatory systems. In particular, NE has also been implicated in novelty-induced learning benefits, specifically in nonhuman animals (Straube et al., 2003b;Sara, 2009; Harley, 2007; Madison and Nicoll, 1986). NE increases the excitability of neurons in the dentate gyrus and promotes long-term potentiation (LTP; Kitchigina et al., 1997; Kemp and Manahan-Vaughn, 2008; Klukowski and Harley, 1994), a mechanism believed to underlie the formation of memories (Cooke and Bliss, 2006).

Several neuromodulatory systems have been suggested to underlie the effects of novelty on learning, such as dopaminergic inputs (Lemon and Manahan-Vaughan, 2006; Li et al., 2003;Lisman and Grace, 2005; Roggenhofer et al., 2010; Sajikumar and Frey, 2004), noradrenergic inputs (Kitchigina et al., 1997; Straube et al., 2003a; Uzakov et al., 2005; Vankov et al., 1995)through beta-adrenoreceptors (Kemp and Manahan-Vaughan,2008), and cholinergic inputs (Barry et al., 2012; Bergado et al.,2007; Hasselmo, 1999; Meeter et al., 2004). The dopaminergic and noradrenergic systems have also been suggested to mediate these effects in concert, working through their reciprocal connections (Briand et al., 2007; Harley, 2004; Sara, 2009). All three neurotransmitters are known to be released in response to novel stimuli, and have been linked to plasticity in the brain.

Another reason to believe that NE nor ACh is crucial for novelty’s effects on memory is the time scale on which the effects occur. Effects of ACh release have been argued to peak some two seconds after release (Hasselmo and Fehlau, 2001), while effects of NE release may act on shorter time scales

Indeed, effects of novel environments one LTP induction have been argued to depend on the activation of dopaminergic D1/D5 receptors (Li et al., 2003).

Such longer-term effects of novelty are most consistent with the idea that DA modulates the novelty-induced benefits for memory, as proposed by, among others, Lisman and Grace (2005). Also other evidence has accumulated for an important role of DA in increasing plasticity in the hippocampus (Jay, 2003; Lemon and Manahan-Vaughan, 2006; Li et al., 2003; Lisman and Grace, 2005; Roggenhofer et al., 2010; Sajikumar and Frey, 2004). Together, these findings suggest that the same mechanism underlies both the benefits of novelty for learning, and the exploration bonus (Düzel et al., 2010; Blumenfeld et al., 2006; Lisman and Grace, 2005).

A framework for organizing novelty’s effects on brainand behavior

In summary, novelty elicits strong responses across a widevariety of brain areas, and stimulates several neuromodulatory systems, affecting many aspects of cognition. Here, we argued that the neurophysiological responses to novelty play out on differenttime-scales, and that this can explain the differences in the timing of novelty’s effects on different cognitive processes. The research reviewed here suggests that these effects can be grouped into atleast three categories. The first two consist of effects that occurs hortly after a novel stimulus is encountered. The third contains longer-lasting effects.

First, the amygdala, mostly known by its role in processing of emotion, responds strongly to novelty as well (Zald, 2003; Blackford et al., 2010). Emotional stimuli are believed to enhancevisual perception by eliciting an attentional response by activating the amygdala and its connections with early visual cortical areas (Vuilleumier, 2005). Since novel stimuli can reliably activate the same brain circuits as emotional stimuli, novelty could potentially enhance perceptual processes via the same pathways. The effects o femotion on visual perception are very fast; although the exact time-course of these effects is not yet known, enhancements are typically reported to occur in the first few hundred milliseconds after presen-tation of an emotional stimulus (Sellinger et al., 2013). Novel stimuli have been shown to have similar enhancing effects on perception (Schomaker and Meeter, 2012). Although much remains uncertain,we argued that the orienting of attention towards novel stimuli mayresult from amygdalar activation affecting early sensory processing regions in the brain.

Second, novel stimuli can activate the LC (a brain stem area thatis the exclusive supplier of NE in the forebrain), resulting in phasic NE release peaking around 200 ms following stimulus presentation (Aston-Jones and Cohen, 2005b; Mongeau et al., 1997). This LC–NE system has been associated with arousal, but can also affect behavior more selectively. The adaptive gain theory (Aston-Jonesand Cohen (2005a) posits that phasic NE release from the LC actsas a temporal filter, facilitating task-relevant behavior by boost-ing decision-making processes and suppressing non-target-relatedbrain activity. Novelty could thus potentially facilitate task perfor-mance via this mechanism. Recent studies showed that new stimulican indeed facilitate responses, but that the effects depend stronglyon other factors. In fact, the speeding of responses seems to be aresponse more to deviance than to novelty per se (Schomaker andMeeter, 2014a). The same has been argued to be the case for thenovelty P3 ERP component (Schomaker et al., 2014c), suggesting apossible common mechanism.

Third, mesolimbic dopaminergic system can be activated by novelty. In contrast with the short-lived LC–NE response, dopaminergic responses elicited by novelty can be effective up to minutes later (Li et al., 2003). After novelty detection, DA release from the SN/VTA is believed to be triggered by a novelty signal from the hippocampus (Lisman and Grace, 2005). Behaviorally, especiall yspatial novelty has been shown to have enhancing effects on memory in animals (Davis et al., 2004; McGaugh, 2005; Uzakov et al.,2005; Straube et al., 2003b), and humans (Fenker et al., 2008; Schomaker et al., 2014b)