A Tradeoff in the Neural Code across Regions and Species.

Many evolutionary years separate humans and macaques, and although the amygdala and cingulate cortex evolved to enable emotion and cognition in both, an evident functional gap exists. Although they were traditionally attributed to differential neuroanatomy, functional differences might also arise from coding mechanisms. Here we find that human neurons better utilize information capacity (efficient coding) than macaque neurons in both regions, and that cingulate neurons are more efficient than amygdala neurons in both species. In contrast, we find more overlap in the neural vocabulary and more synchronized activity (robustness coding) in monkeys in both regions and in the amygdala of both species. Our findings demonstrate a tradeoff between robustness and efficiency across species and regions. We suggest that this tradeoff can contribute to differential cognitive functions between species and underlie the complementary roles of the amygdala and the cingulate cortex. In turn, it can contribute to fragility underlying human psychopathologies.

Shared yet dissociable neural codes across eye gaze, valence and expectation.

The direction of the eye gaze of others is a prominent social cue in primates and is important for communication1-11. Although gaze can signal threat and elicit anxiety6,12,13, it remains unclear whether it shares neural circuitry with stimulus value. Notably, gaze not only has valence, but can also serve as a predictor of the outcome of a social encounter, which can be either negative or positive2,8,12,13. Here we show that the neural codes for gaze and valence overlap in primates and that they involve two different mechanisms: one for the outcome and another for its expectation. Monkeys participated in the human intruder test13,14, in which a human participant had either a direct or averted gaze, interleaved with blocks of aversive and appetitive conditioning. We find that single neurons in the amygdala encode gaze15, whereas neurons in the anterior cingulate cortex encode the social context16, but not gaze. We identify a shared population in the amygdala for which the neural responses to direct and averted gaze parallel the responses to aversive and appetitive stimulus, respectively. Furthermore, we distinguish between two neural mechanisms-an overall-activity scheme that is used for gaze and the unconditioned stimulus, and a correlated-selectivity scheme that is used for gaze and the conditioned stimulus. These findings provide insights into the origins of the neural mechanisms that underlie the computations of both social interactions and valence, and could help to shed light on mechanisms that underlie social anxiety and the comorbidity between anxiety and impaired social interactions.

Two sides of the same amygdala: From shared neural mechanisms to comorbidity of social and affective disorders.

Recent studies identified a circuitry within the primate amygdala that underlies both social and affective processes. Such shared functions within the same circuit, although beneficial for adaptive behavior and make sense in light of evolution, can also contribute to the growing comorbidity between affective and social disorders.

Automatic Recognition of Macaque Facial Expressions for Detection of Affective States.

Internal affective states produce external manifestations such as facial expressions. In humans, the Facial Action Coding System (FACS) is widely used to objectively quantify the elemental facial action units (AUs) that build complex facial expressions. A similar system has been developed for macaque monkeys-the Macaque FACS (MaqFACS); yet, unlike the human counterpart, which is already partially replaced by automatic algorithms, this system still requires labor-intensive coding. Here, we developed and implemented the first prototype for automatic MaqFACS coding. We applied the approach to the analysis of behavioral and neural data recorded from freely interacting macaque monkeys. The method achieved high performance in the recognition of six dominant AUs, generalizing between conspecific individuals (Macaca mulatta) and even between species (Macaca fascicularis). The study lays the foundation for fully automated detection of facial expressions in animals, which is crucial for investigating the neural substrates of social and affective states.