Expectation Modulates Neural Responses to Pleasant and Aversive Stimuli in Primate Amygdala

Abstract

Animals and humans learn to approach and acquire pleasant stimuli and to avoid or defend against aversive ones. However, both pleasant and aversive stimuli can elicit arousal and attention, and their salience or intensity increases when they occur by surprise. Thus, adaptive behavior may require that neural circuits compute both stimulus valence--or value--and intensity. To explore how these computations may be implemented, we examined neural responses in the primate amygdala to unexpected reinforcement during learning. Many amygdala neurons responded differently to reinforcement depending upon whether or not it was expected. In some neurons, this modulation occurred only for rewards or aversive stimuli, but not both. In other neurons, expectation similarly modulated responses to both rewards and punishments. These different neuronal populations may subserve two sorts of processes mediated by the amygdala: those activated by surprising reinforcements of both valences-such as enhanced arousal and attention-and those that are valence-specific, such as fear or reward-seeking behavior.

Neural dynamics underlying impaired autonomic and conditioned responses following amygdala and orbitofrontal lesions.

“…As noted above, the model predicts that these antagonistic rebounds in the LH also shut off the corresponding active drive-value category cells in the AMYG. This is consistent with the observation that cue-and reward-activated AMYG cells are inhibited when expected rewards are omitted (Belova, et al 2007). This AMYG inactivation speeds the extinction of conditioned reinforcer learning from IT a to AMYG, thereby ensuring that changes in cue preference can occur quickly.…”

Dissociable Contributions of Anterior Cingulate Cortex and Basolateral Amygdala on a Rodent Cost/Benefit Decision-Making Task of Cognitive Effort

“…Nor are the effects of BLA inactivation because of indifference between the choices, as choice of the HR option remains far above chance. Unlike previous Pavlovian conditioning experiments (Belova et al, 2007), LR and HR stimuli (levers) carry both appetitive (sucrose reward) and aversive (cognitive effort) predictions, and as such may engage both populations of valencespecific neurons in the BLA, which in turn project to regions such as the NAc. The population-level activity of the BLA may therefore represent the interaction of costs and benefits in a choice, encoding the subjective value of given options, rather than the stimulus properties per se; singlecell recordings from human amygdala strongly support this hypothesis (Jenison et al, 2011).…”

“…Single-cell recordings in primates demonstrate that separate populations of amygdala neurons track positive and negative values of both conditioned and unconditioned stimuli, suggesting that the amygdala encodes a state value for any given moment (Belova et al, 2007(Belova et al, , 2008. In rats, BLA neurons fire more robustly for rewarded vs unrewarded stimuli, and BLA inactivation suppresses animals' responding for reinforced cues .…”

Hebbian and neuromodulatory mechanisms interact to trigger associative memory formation

“…It is known that the LA is involved in both appetitively and aversively motivated learning and that distinct populations of aversive and reward-responsive cells exist in the amygdala (52)(53)(54). One alternate interpretation of our results is that Hebbian mechanisms alone might be sufficient to produce LA plasticity without β-AR activation, but that CS-laser US pairings in the absence of β-AR stimulation produced plasticity in an indiscriminate population of neurons (both aversive and reward-responsive neurons, for example) during learning, some of which generate competing behavioral responses to threat.…”