Elsevier

Neuroscience

Volume 304, 24 September 2015, Pages 71-80
Neuroscience

Functional differences in face processing between the amygdala and ventrolateral prefrontal cortex in monkeys

https://doi.org/10.1016/j.neuroscience.2015.07.047Get rights and content

Highlights

  • Amygdala neurons preferentially responded to facial expressions that are strongly negative.

  • Emotional information of amygdala neurons showed a phasic peak immediately after face presentation onset.

  • Ventrolateral prefrontal cortex neurons preferentially responded to facial expressions with multiple meanings.

  • Emotional information of ventrolateral prefrontal cortex neurons showed a continuous elevation during face presentation.

Abstract

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.

Introduction

Because the ability to categorize social information is essential to survive in a primate’s social group, it is assumed that primates possess neural systems to categorize social information in the brain. Two of several candidates for those systems are located in the amygdala and ventrolateral prefrontal cortex (vlPFC). The primary function of the primate amygdala is emotion processing (LeDoux, 2000, Phelps and LeDoux, 2005), and the amygdala activity is linked with autonomic physiological reactions (Laine et al., 2009). The human amygdala is specifically activated when the subjects see fearful facial expressions (Morris et al., 1996) in addition to body movements of others expressing emotion (Hadjikhani and de Gelder, 2003). Moreover, several researches reported neurons that show different responses to different facial expressions or different directions of gaze of others in the monkey amygdala (Nakamura et al., 1992, Kuraoka and Nakamura, 2006, Kuraoka and Nakamura, 2007, Gothard et al., 2007, Hoffman et al., 2007, Tazumi et al., 2010). On the other hand, neurons in the monkey vlPFC have been reported to respond to faces and vocalizations (Ó Scalaidhe et al., 1997, Sugihara et al., 2006, Tsao et al., 2008, Romanski and Diehl, 2011). There are also neurons that show responses to social behaviors of others in the monkey vlPFC (Tsunada and Sawaguchi, 2012).

The interaction between the amygdala and the vlPFC has recently received attention in relation to emotion regulation (Townsend and Altshuler, 2012). Hariri et al. (2000) reported an increase in regional cerebral blood flow in the right vlPFC during a face cognition task, and a decrease in regional cerebral blood flow in the left and right amygdala. These data imply that the vlPFC regulates emotional responses generated by the amygdala in face perception, through conscious evaluation and appraisal (Hariri et al., 2003).

The primate amygdala and vlPFC are closely related with each other as described above. Then, what are the functional differences in categorizing social information between the amygdala and vlPFC? One candidate for the differences is time of processing. The amygdala has been known to process emotion roughly (Vuilleumier et al., 2003) but rapidly (Balderston et al., 2014). In contrast, neurons in the primate vlPFC have been reported to be involved in complex cognitive functions such as memory (Goldman-Rakic, 1995), behavioral planning (Tanji and Hoshi, 2008) and decision-making (Sakagami and Pan, 2007) that require a little time to be accomplished. Thus, we hypothesized that the role of the amygdala is larger than that of the vlPFC at an early stage of the processing of social information, whereas the role of the vlPFC becomes larger at a late stage.

In the present study, we directly compared neuronal activity between the amygdala and vlPFC of Macaca mulatta during the presentation of face stimuli under the same experimental conditions to elucidate the role of neurons in these two brain regions in face processing. We found rapid phasic peak of information processing about the type of emotion in the amygdala: the information reached a peak of 260 ms after stimulus onset, and maintained more than half of the peak for 170 ms. We also found long-lasting information processing in the vlPFC: the information reached a peak of 630 ms after stimulus onset, and maintained more than half of the peak for 720 ms.

Section snippets

Subjects

We used three rhesus monkeys (M. mulatta, 5–7 kg) for neuron recordings in the amygdala and two rhesus monkeys (5–7 kg) for neuron recordings in the vlPFC. Water was withheld before each daily session and juice was given as a reward in the experimental room. Supplemental water and vegetables were given after the session when needed, and monkey chow was available ad libitum. All experiments were carried out in accordance with the ‘Guide for the Care and Use of Laboratory Animals’ of the National

Results

We recorded the activity of 227 single neurons from the amygdala and 125 single neurons from the vlPFC. Of these, 77 in the amygdala and 61 in the vlPFC were tested on the visual element condition and showed face-responsiveness. The data set from the amygdala neurons comprises the data presented in our previous study (Kuraoka and Nakamura, 2006, Kuraoka and Nakamura, 2007, Kuraoka and Nakamura, 2012), but only the visual element condition is used in this study.

Fig. 1 shows examples of the

Discussion

Neuronal activity is known to encode information about the identity of faces in both the amygdala and the vlPFC (Ó Scalaidhe et al., 1997, Kuraoka and Nakamura, 2006, Gothard et al., 2007, Romanski and Diehl, 2011). However, the neuronal code for different types of emotion has not been examined in the vlPFC, although many studies have reported it in the amygdala (Nakamura et al., 1992, Kuraoka and Nakamura, 2006, Gothard et al., 2007, Hoffman et al., 2007). In this study, we first explicitly

Conclusion

In the present study, we elucidated the functional differences in processing facial expressions between the amygdala and vlPFC in monkeys. In summary, the amygdala neurons rapidly but roughly discriminated the type of facial expressions, and preferentially responded to the strong negative emotional face. By contrast, the vlPFC neurons gradually but stably discriminated the type of facial expressions, and preferentially responded to the face that is difficult to be categorized to a specific

Acknowledgments

This work is supported by Japan Society for the Promotion of Science KAKENHI Grant Number 24700423, Kinki University Research Grant 2013 (to K.K.) and a Grant-in-Aid for Scientific Research on Innovative Areas “Neural creativity for communication (No. 4103)” (21120009) of Ministry of Education, Culture, Sports, Science and Technology, Japan (to K.N.).

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    Present address: Faculty of Medicine, Kinki University, Osaka-Sayama, Osaka 589-8511, Japan.

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