Neuronal responses to face‐like stimuli in the monkey pulvinar

The pulvinar nuclei appear to function as the subcortical visual pathway that bypasses the striate cortex, rapidly processing coarse facial information. We investigated responses from monkey pulvinar neurons during a delayed non‐matching‐to‐sample task, in which monkeys were required to discriminate five categories of visual stimuli [photos of faces with different gaze directions, line drawings of faces, face‐like patterns (three dark blobs on a bright oval), eye‐like patterns and simple geometric patterns]. Of 401 neurons recorded, 165 neurons responded differentially to the visual stimuli. These visual responses were suppressed by scrambling the images. Although these neurons exhibited a broad response latency distribution, face‐like patterns elicited responses with the shortest latencies (approximately 50 ms). Multidimensional scaling analysis indicated that the pulvinar neurons could specifically encode face‐like patterns during the first 50‐ms period after stimulus onset and classify the stimuli into one of the five different categories during the next 50‐ms period. The amount of stimulus information conveyed by the pulvinar neurons and the number of stimulus‐differentiating neurons were consistently higher during the second 50‐ms period than during the first 50‐ms period. These results suggest that responsiveness to face‐like patterns during the first 50‐ms period might be attributed to ascending inputs from the superior colliculus or the retina, while responsiveness to the five different stimulus categories during the second 50‐ms period might be mediated by descending inputs from cortical regions. These findings provide neurophysiological evidence for pulvinar involvement in social cognition and, specifically, rapid coarse facial information processing.     

Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey

There is a population of neurons in the cortex in the middle and anterior part of the superior temporal sulcus (STS) of the monkey with responses which are selective for faces. If, consistent with the effects of damage to the temporal lobe, these neurons are involved in face recognition or in making appropriate social responses to different individuals, then it might be expected that at least some of these neurons might respond differently to different faces. To investigate whether at least some of these neurons do respond differently to different faces, their responses were measured to a standard set of faces, presented in random sequence using a video framestore. It was found that a considerable proportion of the neurons with face selective responses tested (34/44 or 77%) responded differently to different faces, as shown by analyses of variance. An index of the discriminability of the most and least effective face stimulus (d') ranged between 0.2 and 5.0 for the different neurons. Although these neurons often responded differently to different faces, they did not usually respond to only one of the faces in the set, so that information that a particular face had been shown was present across an ensemble of neurons, rather than in the responses of an individual neuron. These findings indicate that the responses of these neurons would be useful in providing information on which different behavioral responses made to different faces could be based. These neurons could thus be filters, the output of which could be used for recognition of different individuals and in emotional responses made to different individuals.     

Categorical representation of objects in the central nucleus of the monkey amygdala

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.     

Impacts of facial identity and type of emotion on responses of amygdala neurons

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.     

Face recognition as a function of social attention in non-human primates: an ERP study

Epidural event related potentials (ERPs) were recorded from four squirrel monkeys (Saimiri sciureus) during the presentation of pictoral stimuli that comprised real human and monkey faces. Subjects viewed tachistoscopically presented stimuli belonging to four different categories: familiar and unfamiliar human faces, and familiar and unfamiliar monkey faces. Familiar faces were subcategorized into top, middle and bottom according to the perceived individual's dominance ranking in a social hierarchy, as rated by human judges observing the group's social behavior. Waveform peak components to monkey and human faces showed similarities in their spatial distribution. However, larger amplitude N1 and N2 components were elicited in response to monkey compared to human faces, particularly over lateral temporo-parietal sites. A similar trend was observed for the P3 component, with maximal differences along midline electrode sites. Responses to familiar and unfamiliar monkey faces showed larger N1s to familiar monkey faces and larger P3s to unfamiliar monkey faces. N1 and P3 components elicited by human faces showed no significant differences between conditions. N2 amplitudes were larger over posterior sites for top-ranked monkeys and larger over frontal sites for middle-and bottom-ranked monkeys. Top-ranked human faces elicited the largest N2 components, middle-ranked faces the next largest, and bottom-ranked faces the smallest. N1, N2, and P3 latencies were similarly sensitive to the ranking of human but not monkey faces. These data suggest that non-human primates exhibit evoked potentials to conspecific and non-conspecific faces that are similar in morphology but different in function. Larger amplitude responses to monkey faces suggests increased processing for that category of stimuli. Additionally, monkey ERPs reflect familiarity with conspecifics but not with human faces. Finally, the social status of the perceived individual, or at least the perceived threat posed by an individual, affects the latencies and magnitudes of ERP components produced by the viewer. These data are consistent with social attention hypotheses which propose that higher status (i.e. more dominant or socially meaningful) members of a group receive more attention than lower status individuals.     

Attention and eye movement related activation of neurons in the dorsal prelunate gyrus (area DP)

Neurons in area DP, the dorsomedial portion of the prelunate gyrus of awake monkeys (Macaca mulatta and Macaca sylvana), responded only little if at all to stationary or moving light stimuli. Circumscribed receptive fields could not be determined in the majority of cells. About 25% of the units became active at a certain gaze position, mostly ipsilateral to the recording site, and with a latency of 70-150 ms after the eye had attained this position with a saccade. About 70% of neurons were activated vigorously when the monkey looked attentively at an object, such as a face, a glove, a hand or simply towards the opening door, and explored it visually. These stimuli elicit attention as well as emotional responses. Photographed objects or faces flashed on a screen produced only little if any response. Our observations, therefore, suggest that the dorsomedial part of the prelunate gyrus may represent activities related to behavioral aspects of vision rather than to features of the visual image itself.     

Visual responses of neurons in the dorsolateral amygdala of the alert monkey

There is evidence that the inferotemporal visual cortex in the monkey projects to the amygdala, and evidence that damage to this region impairs the learning of associations between visual stimuli and reward or punishment. In recordings made in the amygdala to determine whether or not visual responses were found, and if so how they were affected by the significance of the visual stimuli, neurons were found in the dorsolateral part of the amygdala with visual responses which in most cases were sustained while the animal looked at effective visual stimuli. The latency of the responses was 100 to 140 ms or more. The majority (85%) of these neurons responded more strongly to some stimuli than to others, but physical factors which accounted for the responses of the neurons, such as shape, size, orientation, color, or texture, could not usually be identified. Although 22 (19.5%) of these neurons responded primarily to food objects, the responses were not uniquely food-related. Furthermore, although some neurons responded in a visual discrimination test to a visual stimulus which indicated reward, and not to a visual stimulus which indicated saline, only minor modifications of the magnitude of the neuronal responses to the stimuli were obtained when the reward-related significance of the stimuli was reversed. The visual responses of these amygdaloid neurons were thus intermediate in some respects between those of neurons in the inferotemporal cortex, which are not affected by the significance of visual stimuli, and those of neurons in a region to which the amygdala projects, the lateral hypothalamus and substantia innominata, where neurons respond to visual stimuli associated with food reward.     

Time-varying amygdala response to emotional faces in generalized social phobia.

BACKGROUND: Individuals with social phobia (SP) have altered behavioral and neural responses to emotional faces and are hypothesized to have deficits in inhibiting emotion-related amygdala responses. We tested for such amygdala deficits to emotional faces in a sample of individuals with SP. METHOD: We used functional magnetic resonance imaging (fMRI) to examine the neural substrates of emotional face processing in 14 generalized SP (gSP) and 14 healthy comparison (HC) participants. Analyses focused on the temporal dynamics of the amygdala, prefrontal cortex (PFC), and fusiform face area (FFA) across blocks of neutral, fear, contempt, anger, and happy faces in gSP versus HC participants. RESULTS: Amygdala responses in participants with gSP occurred later than the HC participants to fear, angry, and happy faces. Parallel PFC responses were found for happy and fear faces. There were no group differences in temporal response patterns in the FFA. CONCLUSIONS: This finding might reflect a neural correlate of atypical orienting responses among individuals with gSP. Commonly reported SP deficits in habituation might reflect neural regions associated with emotional self-evaluations rather than the amygdala. This study highlights the importance of considering time-varying modulation when examining emotion-related processing in individuals with gSP.     

Comparison of differential neuronal responsiveness for different regions of the prefrontal cortex in a conditional visual discrimination task

To investigate neuronal processing during monkeys' performance of a visual conditional discrimination task, recordings were made from four areas of prefrontal cortex (ventromedial, orbitofrontal, dorsolateral and anterior cingulate) where lesions have been shown to produce impairment of such tasks. Of 1911 recorded neurons, 573 (31%) responded to elements of the task. This proportion was less than the 50% previously reported as responsive in temporal cortex under the same conditions, suggesting sparser encoding in prefrontal than temporal cortex. Of the responsive prefrontal neurons, 165 (29%) responded differently on the different types of trial, so signalling various types of information relevant to task performance and cognition. In line with recent lesion findings, in the dorsolateral region the incidence of such differentially responsive neurons was only an eighth that in the other regions. The relatively high incidence of neuronal responses that encoded a potential instruction cue rather than specific individual stimulus arrangements was consistent with the animals solving the task by using such information, though other neuronal responses could have enabled the task to have been solved by rote learning. Compared to temporal neurons, prefrontal responses more frequently coded information relating to the planned behavioural response rather than perceptual aspects of the task. Population differential response latencies were long (> approximately 225 ms) in prefrontal cortex. A comparison of such differential latencies between temporal and prefrontal cortex indicated that potential information flow was likely to be primarily from temporal to prefrontal cortex rather than vice versa.     

Altered automatic face processing in individuals with high-functioning autism spectrum disorders: Evidence from visual evoked potentials

Individuals with autism spectrum disorders (ASDs) have different automatic responses to faces than typically developing (TD) individuals. We recorded visual evoked potentials (VEPs) in 10 individuals with high-functioning ASD (HFASD) and 10 TD individuals. Visual stimuli consisted of upright and inverted faces (fearful and neutral) and objects presented subliminally in a backward-masking paradigm. In all participants, the occipital N1 (about 100 ms) and P1 (about 120 ms) peaks were major components of the evoked response. We calculated “subliminal face effect (SFE)” scores by subtracting the N1/P1 amplitudes and latencies of the object stimuli from those of the face stimuli. In the TD group, the SFE score for the N1 amplitude was significantly higher for upright fearful faces but not neutral faces, and this score was insignificant when the stimuli were inverted. In contrast, the N1 amplitude of the HFASD subjects did not show this SFE in the upright orientation. There were no significant group differences in SFE scores for P1 amplitude, latency, or N1 latency. Our findings suggest that individuals with HFASD have altered automatic visual processing for emotional faces within the lower level of the visual cortex. This impairment could be a neural component of the disrupted social cognition observed in individuals with HFASD.     

Low spatial frequency filtering modulates early brain processing of affective complex pictures

Recent research on affective processing has suggested that low spatial frequency information of fearful faces provide rapid emotional cues to the amygdala, whereas high spatial frequencies convey fine-grained information to the fusiform gyrus, regardless of emotional expression. In the present experiment, we examined the effects of low (LSF, <15 cycles/image width) and high spatial frequency filtering (HSF, >25 cycles/image width) on brain processing of complex pictures depicting pleasant, unpleasant, and neutral scenes. Event-related potentials (ERP), percentage of recognized stimuli and response times were recorded in 19 healthy volunteers. Behavioral results indicated faster reaction times in response to unpleasant LSF than to unpleasant HSF pictures. Unpleasant LSF pictures and pleasant unfiltered pictures also elicited significant enhancements of P1 amplitudes at occipital electrodes as compared to neutral LSF and unfiltered pictures, respectively; whereas no significant effects of affective modulation were found for HSF pictures. Moreover, mean ERP amplitudes in the time between 200 and 500 ms post-stimulus were significantly greater for affective (pleasant and unpleasant) than for neutral unfiltered pictures; whereas no significant affective modulation was found for HSF or LSF pictures at those latencies. The fact that affective LSF pictures elicited an enhancement of brain responses at early, but not at later latencies, suggests the existence of a rapid and preattentive neural mechanism for the processing of motivationally relevant stimuli, which could be driven by LSF cues. Our findings confirm thus previous results showing differences on brain processing of affective LSF and HSF faces, and extend these results to more complex and social affective pictures.     

Physiological properties of ascending locus coeruleus axons in the squirrel monkey

Discharge activity was recorded extracellularly from individual neurons of the nucleus locus coeruleus in anesthetized squirrel monkeys. These cells exhibited long-duration (2-3 ms) action potentials and discharged spontaneously in a slow (0.2-2 Hz) irregular fashion. Stimulation of the lateral hypothalamus evoked antidromic responses at latencies of 10-20 ms, indicating conduction velocities of over 1 m/s in some cases. The mean refractory period for these axons was 2.6 ms. When the rate of hypothalamic stimulation was increased from 1 to 10 Hz there was a 15-20% increase in antidromic latencies. These properties are similar to those previously observed for rat LC neurons, except that conduction velocities are higher in monkey.     

Increased activation of the anterior cingulate cortex during processing of disgust faces in individuals with social phobia.

BACKGROUND: Researchers have examined the role of differential activation of various brain regions involved in processing emotional information in subjects with social phobia. These studies have focused mostly on the activation of the amygdala. The anterior cingulate cortex (ACC) also has been implicated in processing emotional information, but its role in social phobia has not been examined. METHODS: We recruited subjects with social phobia and matched them with non-anxious control subjects. Participants viewed facial expressions of disgust ("disgust faces") and neutral facial expressions ("neutral faces"). We measured brain activation, focusing on the ACC, using functional magnetic resonance imaging. We also recorded participants' ratings of emotional valence of faces, as well as response latencies to make these valence judgments. We repeated this procedure using three different sets of facial expressions. RESULTS: Individuals with social phobia exhibited a significant increase in ACC activity compared with non-anxious control subjects when processing disgust versus neutral faces. Additionally, compared with control subjects, subjects with social phobia were faster in their ratings of disgust faces and rated the neutral faces more negatively. CONCLUSIONS: Our findings demonstrate that the ACC might be involved in affective processing of negative information in socially phobic subjects.     

Altered fusiform connectivity during processing of fearful faces in social anxiety disorder

Social anxiety disorder (SAD) has been associated with hyper-reactivity in limbic brain regions like the amygdala, both during symptom provocation and emotional face processing tasks. In this functional magnetic resonance imaging study we sought to examine brain regions implicated in emotional face processing, and the connectivity between them, in patients with SAD (n=14) compared with healthy controls (n=12). We furthermore aimed to relate brain reactivity and connectivity to self-reported social anxiety symptom severity. SAD patients exhibited hyper-reactivity in the bilateral fusiform gyrus in response to fearful faces, as well as greater connectivity between the fusiform gyrus and amygdala, and decreased connectivity between the fusiform gyrus and ventromedial prefrontal cortex. Within the SAD group, social anxiety severity correlated positively with amygdala reactivity to emotional faces, amygdala-fusiform connectivity and connectivity between the amygdala and superior temporal sulcus (STS). These findings point to a pivotal role for the fusiform gyrus in SAD neuropathology, and further suggest that altered amygdala-fusiform and amygdala-STS connectivity could underlie previous findings of aberrant socio-emotional information processing in this anxiety disorder.     

Responses of hippocampal formation neurons in the monkey related to delayed spatial response and object-place memory tasks

The memory for where in the environment a particular visual stimulus has been seen is one of the types of memory relatively specifically impaired by hippocampal damage in primates including man. In order to investigate what processing might be performed by the hippocampus related to this type of memory, the activity of hippocampal neurons was recorded while monkeys performed an object-place memory task. In this task, the monkey was shown a sample stimulus in one position on a video screen, there was a delay of 2 s, and then the same or a different stimulus was shown in the same or in a different position. The monkey remembered the sample and its position, and if both matched the delayed stimulus, he licked to obtain fruit juice. Of the 600 neurons analysed in this task, 3.8% responded differently for the different spatial positions, with some of these responding differentially during the sample presentation, some in the delay period, and some in the match period. Thus some hippocampal neurons respond differently for stimuli shown in different positions in space, and some respond differently when the monkey is remembering different positions in space. In addition some of the neurons responded to a combination of object and place information, in that they responded only to a novel object in a particular place. These neuronal responses were not due to any response being made or prepared by the monkey, for information about which behavioral response was required was not available until the match stimulus was shown. This is the first demonstration that some hippocampal neurons in the primate have activity related to the spatial position of stimuli. The activity of these neurons was also measured in a delayed spatial response task, in which the monkey was shown a stimulus in one position, and, after a 2 s delay when two identical stimuli were shown, had to reach to touch the stimulus which was in the position in which it had previously been seen. It was found that the majority of the neurons which responded in the object-place memory task did not respond in the delayed response task. Instead, a different population of neurons (5.7% of the total) responded in the delayed spatial response task, with differential left-right responses in the sample, delay, or match periods.(ABSTRACT TRUNCATED AT 400 WORDS)     

Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging

Brain imaging studies in humans have shown that face processing in several areas is modulated by the affective significance of faces, particularly with fearful expressions, but also with other social signals such gaze direction. Here we review haemodynamic and electrical neuroimaging results indicating that activity in the face-selective fusiform cortex may be enhanced by emotional (fearful) expressions, without explicit voluntary control, and presumably through direct feedback connections from the amygdala. fMRI studies show that these increased responses in fusiform cortex to fearful faces are abolished by amygdala damage in the ipsilateral hemisphere, despite preserved effects of voluntary attention on fusiform; whereas emotional increases can still arise despite deficits in attention or awareness following parietal damage, and appear relatively unaffected by pharmacological increases in cholinergic stimulation. Fear-related modulations of face processing driven by amygdala signals may implicate not only fusiform cortex, but also earlier visual areas in occipital cortex (e.g., V1) and other distant regions involved in social, cognitive, or somatic responses (e.g., superior temporal sulcus, cingulate, or parietal areas). In the temporal domain, evoked-potentials show a widespread time-course of emotional face perception, with some increases in the amplitude of responses recorded over both occipital and frontal regions for fearful relative to neutral faces (as well as in the amygdala and orbitofrontal cortex, when using intracranial recordings), but with different latencies post-stimulus onset. Early emotional responses may arise around 120ms, prior to a full visual categorization stage indexed by the face-selective N170 component, possibly reflecting rapid emotion processing based on crude visual cues in faces. Other electrical components arise at later latencies and involve more sustained activities, probably generated in associative or supramodal brain areas, and resulting in part from the modulatory signals received from amygdala. Altogether, these fMRI and ERP results demonstrate that emotion face perception is a complex process that cannot be related to a single neural event taking place in a single brain regions, but rather implicates an interactive network with distributed activity in time and space. Moreover, although traditional models in cognitive neuropsychology have often considered that facial expression and facial identity are processed along two separate pathways, evidence from fMRI and ERPs suggests instead that emotional processing can strongly affect brain systems responsible for face recognition and memory. The functional implications of these interactions remain to be fully explored, but might play an important role in the normal development of face processing skills and in some neuropsychiatric disorders.     

Autistic traits modulate conscious and nonconscious face perception

Difficulty with emotion perception is a core feature of autism spectrum disorder (ASD) that is also associated with the broader autism phenotype. The current study explored the neural underpinnings of conscious and nonconscious perceptions of affect in typically developing individuals with varying levels of autistic-like traits, as measured by the Autism Quotient (AQ). We investigated the relationship between autistic traits and face processing efficiency using event-related potentials (ERPs). In 20 typically developing adults, we utilized ERPs (the P100, N170, and P300) to measure differences in face processing for emotional faces that were presented either (a) too quickly to reach conscious awareness (16 ms) or (b) slowly enough to be consciously observed (200 ms). All individuals evidenced increased P100 and P300 amplitude and shorter N170 latencies for nonconscious versus consciously presented faces. Individuals with high AQ scores evidenced delayed ERP components. Nonconsciously perceived emotional faces elicited enhanced neural responses regardless of AQ score. Higher levels of autistic traits were associated with inefficient face perception (i.e., longer latency of ERP components). This delay parallels processing delays observed in ASD. These data suggest that inefficient social perception is present in individuals with subclinical levels of social impairment.     

An electrophysiological study of amygdalohypothalamic projections to the ventromedial nucleus of the rat.

The influence of the amygdala on the activity of single neurons within the hypothalamic ventromedial nucleus (HVM) was studied in pentobarbital or urethane anesthetized rats. The results are summarized as follows: (1) Stimulation of different amygdaloid nuclei or of the stria terminalis (ST) evoked a prominent field potential within HVM and altered the spike discharge patterns of the majority of HVM neurons. (2) More than 80% of 428 HVM neurons tested with single amygdala shocks exhibited excitation or excitation-inhibition sequences; the remainder displayed inhibitory responses of 100-150 msec duration at latencies slightly longer than for most of the observed excitatory responses. ST stimulation also evoked excitation or excitation-inhibition sequences from 85% of 240 HVM neurons tested; of the remainder, those with spontaneous activity displayed inhibitory responses with durations of 100-150 msec at latencies slightly longer than for most observed excitatory responses. (3) Evoked potential interaction studies suggested that stimulation of either ST or the amygdala activated the same population of HVM neurons. Single cells tested with both amygdala and ST stimulation displayed similar patterns of response. HVM field potentials and single unit responses to amygdala stimulation were markedly diminished by lesions of ST. Thus, in the rat, only one pathway, i.e., the stria terminalis, contains amygdalofugal fibres to the ventromedial hypothalamic nucleus. (4) The orthodromic responses of HVM neurons were dependent on the frequency of amygdala stimulation. Less than 50% of HVM neurons responded to amygdala stimuli at frequencies greater than 33Hz. Many cells could not be activated at stimulation frequencies greater than 10 Hz, and the spontaneous discharges from certain HVM neurons were effectively abolished at this stimulation frequency. (5) Evidence of prominent postsynaptic inhibition was present throughout HVM. Seventeen HVM neurons displayed amygdala evoked unitary activity different from that of the majority of HVM neurons, and these cells were considered to represent possible inhibitory neurons. In contrast to most HVM neurons activated via probable monosynaptic amygdalohypothalamic pathways, these putative inhibitory neurons were apparently activated via polysynaptic pathways. (6) In summary, these results suggest that the amygdala exerts a prominent monosynaptic influence on the activity of many HVM neurons, coupled with polysynaptic activation of powerful local postsynaptic inhibitory mechanism. In the rat, these amygdala evoked events depend on the integrity of the stria terminalis.     

The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey

Neurophysiological studies have shown that some neurons in the cortex in the superior temporal sulcus and the inferior temporal gyrus of macaque monkeys respond to faces. To determine if facial factors such as expression and identity are encoded independently by face-responsive neurons, 45 neurons were tested on a stimulus set depicting 3 monkeys with 3 expressions each. As tested on a two-way ANOVA, 15 neurons showed response differences to different identities independently of expression, and 9 neurons showed responses to different expressions independently of identity. Three neurons showed significant effects of both factors. Six of the neurons with responses related to expression responded primarily to calm faces, while 2 responded primarily to threat faces. Of a further set of 31 neurons tested on pairs of different expressions, 6 showed strong responses to open-mouth fear or threat expressions, while 2 showed stronger responses to calm faces than threat expressions. Neurons responsive to expression were found primarily in the cortex in the superior temporal sulcus, while neurons responsive to identity were found primarily in the inferior temporal gyrus. The difference in anatomical distribution was statistically significant. This supports the possibility that specific impairments of the recognition of the identity of a face and of its expression in man are due to damage to or disconnection of separate neuronal substrates.     

Activity of primate precentral neurons during voluntary movements triggered by visual signals

Awake, intact monkeys were trained to perform discrete flexion or extension movements of the hand about the wrist in response to visual signals. The object of the movement was to align a cursor, coupled to a manipulandum, on a target line. Cursor and target lines were displayed on a video monitor placed in front of the monkey. The target line was stepped to the right or left, randomly with regard to direction and timing, with each step implying an instruction for the monkey to make a voluntary movement for alignment. Single unit recording was made in the forelimb area of contralateral precentral cortex. Neurons were classified by their responses to passive sensory stimulation and the effects of local intracortical microstimulation into two populations: wrist flexion-extension (F-E) neurons, and all other forelimb neurons (non-wrist (F-E)). A significantly higher proportion of wrist (F-E) neurons as compared to non-wrist (F-E) neurons were task-related. Moreover the wrist (F-E) neurons exhibited exclusively reciprocal responses to the oppositely directed visual signals, whereas the non-wrist (F-E) neurons showed both reciprocal and bidirectional responses. No significant differences in mean latencies of responses, either in respect to the visual signals or to movement onset, were observed between the two populations of neurons. However the range of latencies in both instances was greater in the non-wrist (F-E) populations. The wrist (F-E) population showed significantly less response variability than the non-wrist (F-E) population with regard to response latencies to visual signals and movement onsets, and the degree of correlation between duration of response and reaction time.