Space and Value in the Primate Amygdala and Basal Forebrain

A stimulus predicting reinforcement can trigger emotional responses, such as arousal, as well as cognitive ones, such as increasing attention towards that stimulus. Neuroscientists have long appreciated that the amygdala mediates spatially non-specific emotional responses, but it remains unclear whether the amygdala links motivational and spatial representations in a way that may be important for the emotional-guidance of attention. To test whether amygdala neurons encode spatial and motivational information, we presented reward-predictive cues in different spatial configurations while assessing whether these cues influenced spatial attention. Cue configuration and predicted reward magnitude modulated amygdala neural activity in a coordinated fashion. Moreover, fluctuations in activity were correlated with trial-to-trial variability in spatial attention. Thus the amygdala integrates spatial and motivational information, which may influence the spatial allocation of cognitive resources. When surveying the environment, animals must be acutely aware of associations between stimuli and aversive outcomes in addition to those resulting in appetitive outcomes. This involves attending to appetitive stimuli in order to obtain positive outcomes, and aversive stimuli in order to avoid negative outcomes. While we first demonstrated that amygdala might play a role in influencing spatial attention towards appetitive stimuli, it is unclear whether the activity of individual amygdala neurons are modulated in a similar way by aversive stimuli that also attract attention. Recording from amygdala neurons while monkeys allocated attention both towards appetitive and aversive stimuli revealed that firing rates reflected where attention was allocated irrespective of valence. We also found that amygdala neurons preferentially encode appetitive and aversive stimuli relative to those of little motivational significance in a conditioning paradigm where spatial characteristics were irrelevant. Thus, amygdala neurons respond with respect to the motivational significance of stimuli, which is tied to spatial attention in contexts involving multiple stimuli. While the amygdala might be involved in guiding attention towards motivationally significant stimuli, this process is likely dependent on its interactions with anatomically linked brain areas. The basal forebrain is a candidate brain area for interacting with the amygdala in influencing emotionally-guided attention given its anatomical connectivity and influence over attentional processes. Here, we analyzed data from amygdala and basal forebrain neurons recorded while spatial attention was captured by appetitive and aversive stimuli. Neurons in the basal forebrain were spatial selective for appetitive and aversive stimuli much like the amygdala. We also found that the timing of value signals differed across brain areas in a manner dependent on the spatial configuration of stimuli. Together, these results demonstrate how the amygdala and basal forebrain may participate in coordinating cognitive and emotional processes and are suggestive of how dysfunction within this pathway might contribute to disorders where emotionally-guided attention is impaired.