Neurons responsive to face-view in the primate ventrolateral prefrontal cortex

doi:10.1016/j.neuroscience.2011.05.014

Neuroscience

Volume 189, 25 August 2011, Pages 223-235

https://doi.org/10.1016/j.neuroscience.2011.05.014 Get rights and content

Abstract

Studies have indicated that temporal and prefrontal brain regions process face and vocal information. Face-selective and vocalization-responsive neurons have been demonstrated in the ventrolateral prefrontal cortex (VLPFC) and some prefrontal cells preferentially respond to combinations of face and corresponding vocalizations. These studies suggest VLPFC in nonhuman primates may play a role in communication that is similar to the role of inferior frontal regions in human language processing. If VLPFC is involved in communication, information about a speaker's face including identity, face-view, gaze, and emotional expression might be encoded by prefrontal neurons. In the following study, we examined the effect of face-view in ventrolateral prefrontal neurons by testing cells with auditory, visual, and a set of human and monkey faces rotated through 0°, 30°, 60°, 90°, and −30°. Prefrontal neurons responded selectively to either the identity of the face presented (human or monkey) or to the specific view of the face/head, or to both identity and face-view. Neurons which were affected by the identity of the face most often showed an increase in firing in the second part of the stimulus period. Neurons that were selective for face-view typically preferred forward face-view stimuli (0° and 30° rotation). The neurons which were selective for forward face-view were also auditory responsive compared to other neurons which responded to other views or were unselective which were not auditory responsive. Our analysis showed that the human forward face (0°) was decoded better and also contained the most information relative to other face-views. Our findings confirm a role for VLPFC in the processing and integration of face and vocalization information and add to the growing body of evidence that the primate ventrolateral prefrontal cortex plays a prominent role in social communication and is an important model in understanding the cellular mechanisms of communication.

Highlights

▶Single cell recordings in the awake behaving primate ventrolateral prefrontal cortex to face stimuli differing in gaze/head orientation. ▶Single cells show changes in their neuronal response to different gaze directions. ▶Neurons selective for forward gaze also respond to auditory stimuli. ▶Ventrolateral prefrontal neurons are multisensory and support the notion that this area is involved in communication in the primate brain.

Section snippets

Surgery and electrophysiological recording

We recorded auditory and visual responsive cells in the prefrontal cortex of three naïve rhesus monkeys (Macaca mulatta) that had not yet been tested with combined face and vocalization stimuli. All methods were in accordance with NIH Guidelines for the Care and Use of Laboratory Animals, and the Yale Animal Care and Use Committee Guidelines or the University of Rochester committee on Animal Care and Use. The recording methods have been previously described (Romanski et al., 2005, Sugihara et

General

We examined the response of ventrolateral prefrontal cortex neurons in rhesus macaques as they performed a fixation task for juice reward while presented with auditory or visual stimulus during fixation. During recordings each neuron was first tested with an array of 10 visual stimuli (including objects, faces, and patterns), 10 auditory stimuli (including vocalizations, noise bursts, and other sounds), and the face-view stimulus array (Fig. 1), as described above. Of 301 isolated cells in the

Discussion

In the present study, we have shown that single neurons in the macaque ventral prefrontal cortex (VLPFC) respond differentially to changes in face-view/head orientation. Neurons in the VLPFC responded selectively to either the identity of the face presented (human or macaque) or to the view of the face/head, or to both identity and face-view. Neurons which were affected by the identity of the face most often showed an increase in firing in the second part of the stimulus period. Neurons that

Acknowledgments

The author would like to thank the following individuals for their assistance: M. Pappy, J. Coburn, D. Shannon, and C. Louie for histology; M. Diltz for assistance with figures and comments on the manuscript; and C. Constantinidis for comments on the manuscript.

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Evidence has suggested that the ventrolateral prefrontal cortex (VLPFC) processes social stimuli, including faces and vocalizations, which are essential for communication. Features embedded within audiovisual stimuli, including emotional expression and caller identity, provide abundant information about an individual’s intention, emotional state, motivation, and social status, which are important to encode in a social exchange. However, it is unknown to what extent the VLPFC encodes such features. To investigate the role of VLPFC during social communication, we recorded single-unit activity while rhesus macaques (Macaca mulatta) performed a nonmatch-to-sample task using species-specific face-vocalization stimuli that differed in emotional expression or caller identity. 75% of recorded cells were task-related and of these >70% were responsive during the nonmatch period. A larger proportion of nonmatch cells encoded the stimulus rather than the context of the trial type. A subset of responsive neurons were most commonly modulated by the identity of the nonmatch stimulus and less by the emotional expression, or both features within the face-vocalization stimuli presented during the nonmatch period. Neurons encoding identity were found in VLPFC across a broader region than expression related cells which were confined to only the anterolateral portion of the recording chamber in VLPFC. These findings suggest that, within a working memory paradigm, VLPFC processes features of face and vocal stimuli, such as emotional expression and identity, in addition to task and contextual information. Thus, stimulus and contextual information may be integrated by VLPFC during social communication.
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In fact, the caudal VLPC is connected both with the mouth MN sector, as demonstrated in the present study, and the temporal sectors participating to the visual coding of biological motion and facial expressions, and to the processing of complex auditory stimuli linked to vocalizations (Barbas, 1988; Petrides and Pandya, 2002; Gerbella et al., 2010, 2013; Borra et al., 2011). In agreement with this, VLPC contains neurons responding to visual stimuli of faces and of facial communicative gestures (Ó Scalaidhe et al., 1997, 1999; Sugihara et al., 2006; Romanski and Diehl, 2011; Kuraoka et al., 2015). It is also likely that information related to facial expressions and/or its emotional content could reach the F5/opercular region through other pathways involving the orbitofrontal, insula and the amygdala (see below for further details).
The vast majority of functional studies investigating mirror neurons (MNs) explored their properties in relation to hand actions, and very few investigated how MNs respond to mouth actions or communicative gestures. Since hand and mouth MNs were recorded in two partially overlapping sectors of the ventral precentral cortex of the macaque monkey, there is a general assumption that they share a same neuroanatomical network, with the parietal cortex as a main source of visual information. In the current review, we challenge this perspective and describe the connectivity pattern of mouth MN sector. The mouth MNs F5/opercular region is connected with premotor, parietal areas mostly related to the somatosensory and motor representation of the face/mouth, and with area PrCO, involved in processing gustatory and somatosensory intraoral input. Unlike hand MNs, mouth MNs do not receive their visual input from parietal regions. Such information related to face/communicative behaviors could come from the ventrolateral prefrontal cortex. Further strong connections derive from limbic structures involved in encoding emotional facial expressions and motivational/reward processing. These brain structures include the anterior cingulate cortex, the anterior and mid-dorsal insula, orbitofrontal cortex and the basolateral amygdala. The mirror mechanism is therefore composed and supported by at least two different anatomical pathways: one is concerned with sensorimotor transformation in relation to reaching and hand grasping within the traditional parietal-premotor circuits; the second one is linked to the mouth/face motor control and is connected with limbic structures, involved in communication/emotions and reward processing.
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Working memory is the ability to employ recently seen or heard stimuli and apply them to changing cognitive context. Although much is known about language processing and visual working memory, the neurobiological basis of auditory working memory is less clear. Historically, part of the problem has been the difficulty in obtaining a robust animal model to study auditory short-term memory. In recent years there has been neurophysiological and lesion studies indicating a cortical network involving both temporal and frontal cortices. Studies specifically targeting the role of the prefrontal cortex (PFC) in auditory working memory have suggested that dorsal and ventral prefrontal regions perform different roles during the processing of auditory mnemonic information, with the dorsolateral PFC performing similar functions for both auditory and visual working memory. In contrast, the ventrolateral PFC (VLPFC), which contains cells that respond robustly to auditory stimuli and that process both face and vocal stimuli may be an essential locus for both auditory and audiovisual working memory. These findings suggest a critical role for the VLPFC in the processing, integrating, and retaining of communication information.
This article is part of a Special Issue entitled SI: Auditory working memory.
Specialization of Primate Ventrolateral Prefrontal Cortex for Face and Vocal Processing: Precursor to Communication
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Communication is a multisensory process where information about face identity, emotional expressions, vocalizations, gestures, and mouth movements come together. While many brain regions are involved in this process, the frontal and temporal lobes play important roles in speech and language. Neuroimaging has helped us to localize brain regions for some communication-related functions; nonetheless, our understanding of neuronal activity, specific connections, and precise function are less clear. Thus, it is necessary to utilize animal models to directly record neural activity in these areas to better appreciate the neural basis for these communication-related functions. Macaca mulatta is a species of Old World monkey with a highly developed frontal lobe. In the past 50 years of research utilizing this model, we have learned much about the connections, neurophysiological responses, and functions of the primate prefrontal cortex. Research has shown that one region, in particular, the primate ventrolateral prefrontal cortex (VLPFC) is the recipient of auditory and visual afferents from auditory cortical regions and extrastriate visual regions. This audiovisual recipient zone is located in Brodmann areas 12/47 and 45. In this region neurons respond to complex auditory stimuli, including vocalizations, and to faces. Furthermore, some neurons are multisensory and respond to both auditory and visual stimuli. These multisensory neurons are particularly responsive to macaque vocalizations and their accompanying dynamic facial gestures. VLPFC multisensory neurons are sensitive to the semantic congruency and the temporal synchrony of face and vocalization pairs. Furthermore, neurophysiological recordings show that neurons in this area are active while remembering face and vocalization pairs. Importantly, inactivation of VLPFC results in impaired memory for face and vocalizations. Thus, the nonhuman primate VLPFC is essential in the processing, integration, and remembering of face and vocal stimuli, processes which are critical in communication. The demonstration of a nonhuman primate region that is involved in binding and remembering communication-relevant face and vocal stimuli suggests that this region may be a precursor for the development of frontal lobe language areas in the human brain.
Functional differences in face processing between the amygdala and ventrolateral prefrontal cortex in monkeys
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As stated in our previous study (Kuraoka and Nakamura, 2007), face-responsive neurons in the amygdala were mainly recorded from the lateral, basal, and central nuclei. In this study, we also examined the locations of the recorded vlPFC neurons, and found that face-responsive neurons in the vlPFC were mainly recorded from areas 45 and 12 (Fig. 6), where previous studies have also reported visual responsiveness (Ó Scalaidhe et al., 1997; Sugihara et al., 2006; Romanski and Diehl, 2011). Our recording sites were mainly located in the caudal part of the vlPFC.
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.
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In fact, de-correlation, which increases the amount of information carried by a pool of neurons, at least in the context of the tasks used by these studies, could be even more important given the smaller number of cells that are involved in neural processes in the marmoset. Although the general sources of cortical projections to MT are similar across primates, current evidence suggests that marmoset MT is connected to a greater proportion of the cortex than macaque MT. The extents of the frontal projections are also more extensive, including putative homologues of areas which, in the macaque are usually associated with higher-order multimodal processing, including integration of sensory inputs for social signals and individual identification (e.g. Romanski and Diehl, 2011; Yeterian et al., 2012). The interconnections with the ventral stream also appear to be more abundant than those observed in the macaque.
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Cognitive, Behavioral, and Systems NeuroscienceResearch PaperNeurons responsive to face-view in the primate ventrolateral prefrontal cortex

Abstract

Highlights

Section snippets

Surgery and electrophysiological recording

General

Discussion

Acknowledgments

Brain Res Bull

Neuron

Neuroimage

Neuropsychologia

Cognition

Behav Brain Res

Biol Psychiatry

Curr Biol

Brain Res Bull

Brain Res Cogn Brain Res

Neurosci Res

Curr Biol

Behav Brain Res

Cognition

Neuroimage

Neuroimage

Neuroimage

Neuroscience

Vis Res

Cogn Sci

Neuron

Behav Brain Res

Neuron

Neural activity in prefrontal cortex during copying geometrical shapes. II. Decoding shape segments from neural ensembles

Exp Brain Res

Flow of information for emotions through temporal and orbitofrontal pathways

J Anat

Architecture and cortical connections of the prefrontal cortex in the rhesus monkey

Adv Neurol

Information theory and neural coding

Nat Neurosci

Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys

J Comp Neurol

The amygdala: vigilance and emotion

Mol Psychiatry

Distinct temporal lobe projections to auditory and visual regions in the ventral prefrontal cortex support face and vocalization processing

Neuronal correlates of face identification in the monkey anterior temporal cortical areas

J Neurophysiol

Functional compartmentalization and viewpoint generalization within the macaque face-processing system

Science

How well can we estimate the information carried in neuronal responses from limited samples?

Neural Comput

Neural responses to facial expression and face identity in the monkey amygdala

J Neurophysiol

Multiple perceptual strategies used by macaque monkeys for face recognition

Anim Cogn

Eye contact and face scanning in early infancy

Science

Neural interaction of the amygdala with the prefrontal and temporal cortices in the processing of facial expressions as revealed by fMRI

J Cogn Neurosci

Repetition suppression of faces is modulated by emotion

Proc Natl Acad Sci U S A

Applied multivariate statistical analysis

Cognitive, Behavioral, and Systems Neuroscience
Research Paper
Neurons responsive to face-view in the primate ventrolateral prefrontal cortex