Conditioned appetitive and aversive responses (CRs) are thought to result from the activation of specific subsets of valence-coding basolateral amygdala (BLA) neurons. Under this model, the responses of BLA cells to conditioned stimuli (CSs) and the activity that drives CRs are closely related. We tested the strength of this correlation using a task where rats could emit different CRs in response to the same CSs. At odds with this model, the CS responses and CR-related activity of individual BLA cells were separable. Moreover, while the incidence of valence-coding cells did not exceed chance, at the population level there was similarity between valence coding for CSs and CRs. In fact, both lateral and basolateral neurons concurrently encoded multiple task features and behaviors. Thus, conditioned emotional behaviors may not depend on the recruitment of single cells that explicitly encode individual task variables but from multiplexed representations distributed across the BLA.

No abstract

Fear conditioning studies have led to the view that the amygdala contains neurons that signal threat and in turn elicit defensive behaviors through their brain stem and hypothalamic targets. In agreement with this model, a prior unit-recording study in rats performing a seminaturalistic foraging task revealed that many lateral amygdala (LA) neurons are predator responsive. In contrast, our previous study emphasized that most basolateral (BL) amygdala neurons are inhibited at proximity of the predator. However, the two studies used different methods to analyze unit activity, complicating comparisons between them. By applying the same method to the sample of BL neurons we recorded previously, the present study revealed that most principal cells are inhibited by the predator and only 4.5% are activated. Moreover, two-thirds of these cells were also activated by nonthreatening stimuli. In fact, fitting unit activity with a generalized linear model revealed that the only task variables associated with a prevalent positive modulation of BL activity were expectation of the predator’s presence and whether the prior trial had been a failure or success. At odds with the threat-coding model of the amygdala, actual confrontation with the predator was usually associated with a widespread inhibition of principal BL neurons. NEW & NOTEWORTHY The basolateral amygdala (BL) is thought to contain neurons that signal threat, in turn eliciting defensive behaviors. In contrast, the present study reports that very few principal BL cells are responsive to threats and that most of them are also activated by nonthreatening stimuli. Yet, expectation of the threat’s presence was associated with a prevalent positive modulation of BL activity; actual confrontation with the threat was associated with a widespread inhibition.

Highlights d Neurons in LA, BL, and PL encode the same set of emotional variables d BL and PL neurons tend to encode more events with minor changes in firing rate d LA neurons tend to encode fewer events with larger changes in firing rate d LA and BL populations encode valence, while PL encodes trial identity

The lateral (LA) and basolateral (BL) nuclei of the amygdala regulate emotional behaviors. Despite their dissimilar extrinsic connectivity, they are often combined, perhaps because their cellular composition is similar to that of the cerebral cortex, including excitatory principal cells reciprocally connected with fast-spiking interneurons (FSIs). In the cortex, this microcircuitry produces gamma oscillations that support information processing and behavior. We tested whether this was similarly the case in the rat (males) LA and BL using extracellular recordings, biophysical modeling, and behavioral conditioning. During periods of environmental assessment, both nuclei exhibited gamma oscillations that stopped upon initiation of active behaviors. Yet, BL exhibited more robust spontaneous gamma oscillations than LA. The greater propensity of BL to generate gamma resulted from several microcircuit differences, especially the proportion of FSIs and their interconnections with principal cells. Furthermore, gamma in BL but not LA regulated the efficacy of excitatory synaptic transmission between connected neurons. Together, these results suggest fundamental differences in how LA and BL operate. Most likely, gamma in LA is externally driven, whereas in BL it can also arise spontaneously to support ruminative processing and the evaluation of complex situations.