Abstract Decision-making is influenced by both expected reward and social factors, such as who offered the outcomes. Thus, although a reward might originally be independent from social factors, the two elements are closely related. However, whether and how they are processed separately or conjointly remains unclear. Here, we show that neurons in distinct sub-nuclei of the amygdala encode expected reward and face animacy, which is a vital aspect of face perception. Although these encoding processes are distinct, they rely on partially shared neuronal circuits with characteristic temporal dynamics. Two male macaque monkeys made saccades under different social and reward contexts, created by presenting facial images with independent attributes: animacy (a monkey or cartoon face) and associated reward (large or small). The stimulus image was presented twice per trial: during the initial stimulus encoding (S1) and before saccades were made (S2). A longer gaze duration for eye region of the monkey versus cartoon images indicated more robust social engagement for realistic faces. During S1, a similar number of lateral nucleus neurons encoded either animacy only with a monkey-image preference, reward only with a large-reward preference, or both. Conversely, neurons in the basal and central nuclei primarily encoded reward, preferring large-versus small-reward associated face images. The reward-dependent modulation was continuous after S1, but was more conspicuous during S1 in the basal nucleus and during both S1 and S2 in the central nucleus. This anatomically- and temporally-specific encoding in the amygdala may underlie the computation and integration of face animacy and reward information. Significance Statement Reward and social information are closely related but originally independent, as both influence our decision-making. The amygdala has been associated with both reward and social information coding. However, whether and how they are processed separately or conjointly by individual neurons in the amygdala remains unclear. We found that neurons in the lateral and basal nuclei encoded face animacy, which is an important aspect of social information, and reward, respectively, during sensory processing. Neurons in the central nucleus encoded reward information during the execution phase. This provides new clarity regarding the mechanisms of separate or integrated social and reward information processing within the amygdala.

The ability to categorize social information is essential to survive in a primate's social group. In the monkey brain, there are neural systems to categorize social information. Among these, the relationship between the amygdala and the ventrolateral prefrontal cortex (vlPFC) has recently gained focus with regard to emotion regulation. However, the processing of facial information and the functional differences in these two areas remain unclear. Thus, in this study, we examined the response properties of single neurons in the amygdala and vlPFC while presenting video clips of three types of facial emotions (aggressive threat, coo, and scream) in Macaca mulatta. Neurons in the amygdala were preferentially activated upon presentation of a scream facial expression, which is strongly negative, whereas the neurons in the vlPFC were activated upon presentation of coo, a facial expression with multiple meanings depending on the social context. Information analyses revealed that the amount of information conveyed by the amygdala neurons about the type of emotion transiently increased immediately after stimulus presentation. In contrast, the information conveyed by the vlPFC neurons showed sustained elevation during stimulus presentation. Therefore, our results suggest that the amygdala processes strong emotion roughly but rapidly, whereas the vlPFC spends a great deal of time processing ambiguous facial information in communication, and make an accurate decision from multiple possibilities based on memory. (C) 2015 IBRO. Published by Elsevier Ltd. All rights reserved.

Rhythm is an essential element of human culture, particularly in language and music. To acquire language or music, we have to perceive the sensory inputs, organize them into structured sequences as rhythms, actively hold the rhythm information in mind, and use the information when we reproduce or mimic the same rhythm. Previous brain imaging studies have elucidated brain regions related to the perception and production of rhythms. However, the neural substrates involved in the working memory of rhythm remain unclear. In addition, little is known about the processing of rhythm information from non-auditory inputs (visual or tactile). Therefore, we measured brain activity by functional magnetic resonance imaging while healthy subjects memorized and reproduced auditory and visual rhythmic information. The inferior parietal lobule, inferior frontal gyrus, supplementary motor area, and cerebellum exhibited significant activations during both encoding and retrieving rhythm information. In addition, most of these areas exhibited significant activation also during the maintenance of rhythm information. All of these regions functioned in the processing of auditory and visual rhythms. The bilateral inferior parietal lobule, inferior frontal gyrus, supplementary motor area, and cerebellum are thought to be essential for motor control. When we listen to a certain rhythm, we are often stimulated to move our body, which suggests the existence of a strong interaction between rhythm processing and the motor system. Here, we propose that rhythm information may be represented and retained as information about bodily movements in the supra-modal motor brain system.

The primate amygdala consists of several subnuclei. Neurons in this brain area have been known to respond to stimuli belonging to specific categories of objects, such as faces, animals, and artifacts. However, little is known about the functional differences among the nuclei of the primate amygdala. To clarify functional differences among these subnuclei in object categorization, we compared the responsiveness of neuronal populations among the lateral, basal and central nuclei of the monkey amygdala. The activity of 203 neurons was recorded while video clips of 13 stimuli belonging to three categories (monkey, human, and artifact) were presented. Of these neurons, 37, 39 and 37 neurons in the lateral, basal and central nuclei, respectively, responded to at least one of the stimuli. We applied a cluster analysis to the neuronal population responses from these nuclei, and also calculated information about the three categories and monkey identity from each neuronal population. We found that the three categories and monkey identity could be more properly classified by neuronal responsiveness in the central nucleus, which is an output gate of the amygdala, than by that in the lateral and basal nuclei. These results suggest that the information about objects suitable for the generation of appropriate emotional response is built up within the primate amygdala via an intra-amygdala network from the lateral nucleus to the central nucleus.

Using an infrared thermographic system, we have demonstrated, as previously reported, that temperatures in the nasal region of macaque monkeys decrease during negative emotional states, such as when facing a threatening person. In this study, we explored the usefulness of measuring nasal skin temperatures in studies of monkey emotions as manifested by conspecific emotional behaviors and expressions. We measured nasal skin temperatures of rhesus monkeys (Macaca mulatto) in response to video clips, all showing monkeys: a raging individual (Experiment 1), three distinct emotional expressions (Experiment 2), and only faces or voices representing a threat (Experiment 3). We found that nasal skin temperatures significantly decreased in response to a threatening stimulus, even when the stimulus was a 20 image with digitized sound, similar to those used in many psychological or neurophysiological studies on animal emotion. Moreover, species-specific aggressive threats invariably elicited a decrease in nasal skin temperatures and skin conductance responses; however, screams or coos did not elicit this response. Simultaneous perception of both facial expressions and vocalizations induced a more prominent decrease in nasal skin temperatures than did the perception of facial expressions or vocalizations alone. Taken together, these data suggest that decreased nasal skin temperatures should be added to the list of indicators of emotional states in animals. (C) 2010 Elsevier Inc. All rights reserved.

The face and voice can independently convey the same information about emotion. When we see an angry face or hear an angry voice, we can perceive a person's anger. These two different sensory cues are interchangeable in this sense. However, it is still unclear whether the same group of neurons process signals for facial and vocal emotions. We recorded neuronal activity in the amygdala of monkeys while watching nine video clips of species-specific emotional expressions: three monkeys showing three emotional expressions (aggressive threat, scream, and coo). Of the 227 amygdala neurons tested, 116 neurons (51%) responded to at least one of the emotional expressions. These "monkey-responsive" neurons - that is, neurons that responded to monkey-specific emotional expression - preferred the scream to other emotional expressions irrespective of identity. To determine the element crucial to neuronal responses, the activity of 79 monkey-responsive neurons was recorded while a facial or vocal element of a stimulus was presented alone. Although most neurons (61/79, 77%) strongly responded to the visual but not to the auditory element, about one fifth (16/79, 20%) maintained a good response when either the facial or vocal element was presented. Moreover, these neurons maintained their stimulus-preference profiles under facial and vocal conditions. These neurons were found in the central nucleus of the amygdala, the nucleus that receives inputs from other amygdala nuclei and in turn sends outputs to other emotion-related brain areas. These supramodal responses to emotion would be of use in generating appropriate responses to information regarding either facial or vocal emotion.

The amygdala has been implicated in the processing of emotional expressions. Who makes the emotion and the type of emotion are important in producing appropriate responses. How amygdala neurons are affected by facial identity and type of emotion, however, has not yet been systematically examined. We examined the activity of amygdala neurons using nine monkey stimuli: 3 monkeys x 3 types of emotion. Of the 227 neurons tested, 77 responded to the monkey stimuli. The effects of facial identity and type of emotion on the response magnitude were significant in 48 and 57 neurons, respectively. Both effects were significant in 38 neurons. These results indicate that both facial identity and type of emotion have strong impacts on amygdala functions.

We established an infrared thermographic system for the detection of emotion-related temperature changes in rhesus monkeys (Macaca mulatta). We continuously measured temperatures of various facial regions of four rhesus monkeys during the presentation of a potentially 'threatening' person, i.e., a person in a laboratory coat with a catching net, who entered the experimental room and approached the monkeys. The temperatures were also measured before and after the presentation of the 'stimulation period.' The temperature of the nasal region decreased significantly within 10-30 s, and continued to decrease throughout the stimulation period. During this period, the monkeys frequently expressed silent bared-teeth face, staring open-mouth face, and lip-smacking, all of which were expressions of a negative emotion. Assuming that the monkeys experience the negative emotion when viewing the potentially threatening stimulus, we conclude that the decrease in nasal skin temperature is relevant to the alteration of the emotional state. The present findings suggest that nasal temperature can be a reliable and accurate indicator of a change from neutral to negative in emotional state of non-human primates. (c) 2005 Elsevier Inc. All rights reserved.

We trained 2 monkeys to display facial actions in response to corresponding arbitrary visual cues. Each monkey executed the task successfully, and each displayed two different facial actions corresponding to either hand-sign or color cues. More than 90% of the responses were correct for each monkey. These results provide evidence that monkeys can execute facialactions in response to conditioned visual cues in the absence of social context. These data suggest that facial actions of monkeys are flexible enough for use in further laboratory investigations-for example, in studies on the neural mechanisms underlying the execution of actions.