Monkey Temporal Cortex Research Articles

The impact of stimulus size and orientation on individual face coding in monkey face-selective cortex

Face-selective neurons in the monkey temporal cortex discharge at different rates in response to pictures of different individual faces. Here we tested whether this pattern of response across single neurons in the face-selective area ML (located in the middle Superior Temporal Sulcus) tolerates two affine transformations; picture-plane inversion, known to decrease the average response of face-selective neurons and the other, stimulus size. We recorded the response of 57 ML neurons in two awake and fixating monkeys. Face stimuli were presented at two sizes (10 and 5 degrees of visual angle) and two orientations (upright and inverted). Different faces elicited distinct patterns of activity across ML neurons that were reliable (i.e., predictable with a classifier) within a specific size and orientation condition. Despite observing a reduction in the average response magnitude of face-selective neurons to inverted faces, compared to upright faces, classifier performance was above chance for both upright and inverted faces. While decoding was largely preserved across changes in stimulus size, a classifier trained with one orientation condition and tested on the other did not lead to performance above chance level. We conclude that different individual faces can be decoded from patterns of responses in the monkey area ML regardless of orientation or size, but with qualitatively different patterns of responses for upright and inverted faces.

Grandmother cells: much ado about nothing

ABSTRACTWe do not dispute the possibility of the existence in the brain of “grandmother cells”, which are very finely tuned neurons that fire only in the presence of specific objects or categories. However, we question the causal efficacy of such neurons at the functional or behaviour level. We claim that, even though very familiar items, such as “my grandmother”, may well have associated grandmother neurons, these neurons have very little, or no impact on the actual recognition of my grandmother. A study by Thomas, Van Hulle, and Vogels [(2002). Encoding of categories by noncategory-specific neurons in the inferior temporal cortex. Journal of Cognitive Neuroscience, 13, 190–200. doi:10.1162/089892901564252] found finely tuned, category-specific neurons in the inferior temporal cortex of monkeys, but also found that when these neurons were removed from their analysis, this had no effect on categorisation performance. Further, we have found no reported cases of the loss of recognition of single, highly familiar objects, which also argues for a lack of causal efficacy of grandmother-cell neurons.

Laminar Module Cascade from Layer 5 to 6 Implementing Cue-to-Target Conversion for Object Memory Retrieval in the Primate Temporal Cortex

The cerebral cortex computes through the canonical microcircuit that connects six stacked layers; however, how cortical processing streams operate invivo, particularly in the higher association cortex, remains elusive. By developing a novel MRI-assisted procedure that reliably localizes recorded single neurons at resolution of six individual layers in monkey temporal cortex, we show that transformation of representations from a cued object to a to-be-recalled object occurs at the infragranular layer in a visual cued-recall task. This cue-to-target conversion started in layer 5 and was followed by layer 6. Finally, a subset of layer 6 neurons exclusively encoding the sought target became phase-locked to surrounding field potentials at theta frequency, suggesting that this coordinated cell assembly implements cortical long-distance outputs of the recalled target. Thus, this study proposes a link from local computation spanning laminar modules of the temporal cortex to the brain-wide network for memory retrieval in primates.

Top-Down Regulation of Laminar Circuit via Inter-Area Signal for Successful Object Memory Recall in Monkey Temporal Cortex

Memory retrieval in primates is orchestrated by a brain-wide neuronal circuit. To elucidate the operation of this circuit, it is imperative to comprehend neuronal mechanisms of coordination between area-to-area interaction and information processing within individual areas. By simultaneous recording from area 36 (A36) and area TE (TE) of the temporal cortex while monkeys performed a pair-association memory task, we found two distinct inter-area signal flows during memory retrieval: A36 spiking activity exhibited coherence with low-frequency field activity in either the supragranular or infragranular layer of TE. Of these two flows, only signal flow targeting the infragranular layer of TE was further translaminarly coupled with gamma activity in the supragranular layer of TE. Moreover, this coupling was observed when monkeys succeeded in the retrieval of the sought object but not when they failed. The results suggest that local translaminar processing can be recruited via a layer-specific inter-area network for memory retrieval.

Dissimilar processing of emotional facial expressions in human and monkey temporal cortex.

Emotional facial expressions play an important role in social communication across primates. Despite major progress made in our understanding of categorical information processing such as for objects and faces, little is known, however, about how the primate brain evolved to process emotional cues. In this study, we used functional magnetic resonance imaging (fMRI) to compare the processing of emotional facial expressions between monkeys and humans. We used a 2×2×2 factorial design with species (human and monkey), expression (fear and chewing) and configuration (intact versus scrambled) as factors. At the whole brain level, neural responses to conspecific emotional expressions were anatomically confined to the superior temporal sulcus (STS) in humans. Within the human STS, we found functional subdivisions with a face-selective right posterior STS area that also responded to emotional expressions of other species and a more anterior area in the right middle STS that responded specifically to human emotions. Hence, we argue that the latter region does not show a mere emotion-dependent modulation of activity but is primarily driven by human emotional facial expressions. Conversely, in monkeys, emotional responses appeared in earlier visual cortex and outside face-selective regions in inferior temporal cortex that responded also to multiple visual categories. Within monkey IT, we also found areas that were more responsive to conspecific than to non-conspecific emotional expressions but these responses were not as specific as in human middle STS. Overall, our results indicate that human STS may have developed unique properties to deal with social cues such as emotional expressions.

Prevalence of Selectivity for Mirror-Symmetric Views of Faces in the Ventral and Dorsal Visual Pathways

Although the ability to recognize faces and objects from a variety of viewpoints is crucial to our everyday behavior, the underlying cortical mechanisms are not well understood. Recently, neurons in a face-selective region of the monkey temporal cortex were reported to be selective for mirror-symmetric viewing angles of faces as they were rotated in depth (Freiwald and Tsao, 2010). This property has been suggested to constitute a key computational step in achieving full view-invariance. Here, we measured functional magnetic resonance imaging activity in nine observers as they viewed upright or inverted faces presented at five different angles (-60, -30, 0, 30, and 60°). Using multivariate pattern analysis, we show that sensitivity to viewpoint mirror symmetry is widespread in the human visual system. The effect was observed in a large band of higher order visual areas, including the occipital face area, fusiform face area, lateral occipital cortex, mid fusiform, parahippocampal place area, and extending superiorly to encompass dorsal regions V3A/B and the posterior intraparietal sulcus. In contrast, early retinotopic regions V1-hV4 failed to exhibit sensitivity to viewpoint symmetry, as their responses could be largely explained by a computational model of low-level visual similarity. Our findings suggest that selectivity for mirror-symmetric viewing angles may constitute an intermediate-level processing step shared across multiple higher order areas of the ventral and dorsal streams, setting the stage for complete viewpoint-invariant representations at subsequent levels of visual processing.

Distinct Mechanisms for Coding of Visual Actions in Macaque Temporal Cortex

Temporal cortical neurons are known to respond to visual dynamic-action displays. Many human psychophysical and functional imaging studies examining biological motion perception have used treadmill walking, in contrast to previous macaque single-cell studies. We assessed the coding of locomotion in rhesus monkey (Macaca mulatta) temporal cortex using movies of stationary walkers, varying both form and motion (i.e., different facing directions) or varying only the frame sequence (i.e., forward vs backward walking). The majority of superior temporal sulcus and inferior temporal neurons were selective for facing direction, whereas a minority distinguished forward from backward walking. Support vector machines using the temporal cortical population responses as input classified facing direction well, but forward and backward walking less so. Classification performance for the latter improved markedly when the within-action response modulation was considered, reflecting differences in momentary body poses within the locomotion sequences. Responses to static pose presentations predicted the responses during the course of the action. Analyses of the responses to walking sequences wherein the start frame was varied across trials showed that some neurons also carried a snapshot sequence signal. Such sequence information was present in neurons that responded to static snapshot presentations and in neurons that required motion. Our data suggest that actions are analyzed by temporal cortical neurons using distinct mechanisms. Most neurons predominantly signal momentary pose. In addition, temporal cortical neurons, including those responding to static pose, are sensitive to pose sequence, which can contribute to the signaling of learned action sequences.

Effects of long term image familiarity in monkey temporal cortex

Effects of long term image familiarity in monkey temporal cortex

Multineuronal vectorization is more efficient than time-segmental vectorization for information extraction from neuronal activities in the inferior temporal cortex

In order for patients with disabilities to control assistive devices with their own neural activity, multineuronal spike trains must be efficiently decoded because only limited computational resources can be used to generate prosthetic control signals in portable real-time applications. In this study, we compare the abilities of two vectorizing procedures (multineuronal and time-segmental) to extract information from spike trains during the same total neuron-seconds. In the multineuronal vectorizing procedure, we defined a response vector whose components represented the spike counts of one to five neurons. In the time-segmental vectorizing procedure, a response vector consisted of components representing a neuron's spike counts for one to five time-segment(s) of a response period of 1 s. Spike trains were recorded from neurons in the inferior temporal cortex of monkeys presented with visual stimuli. We examined whether the amount of information of the visual stimuli carried by these neurons differed between the two vectorizing procedures. The amount of information calculated with the multineuronal vectorizing procedure, but not the time-segmental vectorizing procedure, significantly increased with the dimensions of the response vector. We conclude that the multineuronal vectorizing procedure is superior to the time-segmental vectorizing procedure in efficiently extracting information from neuronal signals.

Temporal Cortex Neurons Encode Articulated Actions as Slow Sequences of Integrated Poses

Form and motion processing pathways of the primate visual system are known to be interconnected, but there has been surprisingly little investigation of how they interact at the cellular level. Here we explore this issue with a series of three electrophysiology experiments designed to reveal the sources of action selectivity in monkey temporal cortex neurons. Monkeys discriminated between actions performed by complex, richly textured, rendered bipedal figures and hands. The firing patterns of neurons contained enough information to discriminate the identity of the character, the action performed, and the particular conjunction of action and character. This suggests convergence of motion and form information within single cells. Form and motion information in isolation were both sufficient to drive action discrimination within these neurons, but removing form information caused a greater disruption to the original response. Finally, we investigated the temporal window across which visual information is integrated into a single pose (or, equivalently, the timing with which poses are differentiated). Temporal cortex neurons under normal conditions represent actions as sequences of poses integrated over approximately 120 ms. They receive both motion and form information, however, and can use either if the other is absent.

Seeing the future: Natural image sequences produce “anticipatory” neuronal activity and bias perceptual report

This paper relates human perception to the functioning of cells in the temporal cortex that are engaged in high-level pattern processing. We review historical developments concerning (a) the functional organization of cells processing faces and (b) the selectivity for faces in cell responses. We then focus on (c) the comparison of perception and cell responses to images of faces presented in sequences of unrelated images. Specifically the paper concerns the cell function and perception in circumstances where meaningful patterns occur momentarily in the context of a naturally or unnaturally changing visual environment. Experience of visual sequences allows anticipation, yet one sensory stimulus also "masks" perception and neural processing of subsequent stimuli. To understand this paradox we compared cell responses in monkey temporal cortex to body images presented individually, in pairs and in action sequences. Responses to one image suppressed responses to similar images for approximately 500 ms. This suppression led to responses peaking 100 ms earlier to image sequences than to isolated images (e.g., during head rotation, face-selective activity peaks before the face confronts the observer). Thus forward masking has unrecognized benefits for perception because it can transform neuronal activity to make it predictive during natural change.

Object Representations in the Temporal Cortex of Monkeys and Humans as Revealed by Functional Magnetic Resonance Imaging

Increasing evidence suggests that the neural processes associated with identifying everyday stimuli include the classification of those stimuli into a limited number of semantic categories. How the neural representations of these stimuli are organized in the temporal lobe remains under debate. Here we used functional magnetic resonance imaging (fMRI) to identify correlates for three current hypotheses concerning object representations in the inferior temporal (IT) cortex of monkeys and humans: representations based on animacy, semantic categories, or visual features. Subjects were presented with blocked images of faces, body parts (animate stimuli), objects, and places (inanimate stimuli), and multiple overlapping contrasts were used to identify the voxels most selective for each category. Stimulus representations appeared to segregate according to semantic relationships. Discrete regions selective for animate and inanimate stimuli were found in both species. These regions could be further subdivided into regions selective for individual categories. Notably, face-selective regions were contiguous with body-part-selective regions, and object-selective regions were contiguous with place-selective regions. When category-selective regions in monkeys were tested with blocks of single exemplars, individual voxels showed preferences for visually dissimilar exemplars from the same category and voxels with similar preferences tended to cluster together. Our results provide some novel observations with respect to how stimulus representations are organized in IT cortex. In addition, they further support the idea that representations of complex stimuli in IT cortex are organized into multiple hierarchical tiers, encompassing both semantic and physical properties.

Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex

The ability to perceive and differentiate facial expressions is vital for social communication. Numerous functional MRI (fMRI) studies in humans have shown enhanced responses to faces with different emotional valence, in both the amygdala and the visual cortex. However, relatively few studies have examined how valence influences neural responses in monkeys, thereby limiting the ability to draw comparisons across species and thus understand the underlying neural mechanisms. Here we tested the effects of macaque facial expressions on neural activation within these two regions using fMRI in three awake, behaving monkeys. Monkeys maintained central fixation while blocks of different monkey facial expressions were presented. Four different facial expressions were tested: (i) neutral, (ii) aggressive (open-mouthed threat), (iii) fearful (fear grin), and (iv) submissive (lip smack). Our results confirmed that both the amygdala and the inferior temporal cortex in monkeys are modulated by facial expressions. As in human fMRI, fearful expressions evoked the greatest response in monkeys-even though fearful expressions are physically dissimilar in humans and macaques. Furthermore, we found that valence effects were not uniformly distributed over the inferior temporal cortex. Surprisingly, these valence maps were independent of two related functional maps: (i) the map of "face-selective" regions (faces versus non-face objects) and (ii) the map of "face-responsive" regions (faces versus scrambled images). Thus, the neural mechanisms underlying face perception and valence perception appear to be distinct.

Impairment in object-in-place scene learning after uncinate fascicle section in macaque monkeys.

Three previous experiments have shown that a disconnection of frontal cortex from inferior temporal cortex in monkeys impairs a variety of visual learning tasks but leaves concurrent object discrimination learning intact. In the present experiment, three monkeys were trained on an object-in-place task where concurrent object discrimination learning took place within unique background scenes. After surgery to transect the uncinate fascicle, the monosynaptic route between prefrontal cortex and inferior temporal cortex, all three monkeys showed an impairment relative to their preoperative performance. Combined with previously reported impairments after uncinate fascicle transection, the interaction between frontal cortex and inferotemporal cortex is likely to be important in discrimination learning in background scenes because learning depends on associating the visual elements of a scene together with the appropriate choice object. This result adds to recent evidence showing that tasks such as object-in-place learning and conditional learning are impaired after disconnection of frontal cortex from inferior temporal cortex because those tasks require the representation of temporally extended events.

Confocal mapping of cortical inputs onto identified pyramidal neurons

Using a confocal microscopy protocol, we carried out a microcircuitry investigation of cortical connections in monkey temporal cortex. Inputs were labeled by BDA injections in posterior area TE, and potential postsynaptic pyramidal neuron targets were labeled with EGFP, by injection of retrogradely transported adenovirus. We scored the number and distribution of putative contacts onto dendritic compartments of neurons in different layers. Initial results show that about 50 percent of apical dendrites of layer (L.) 6 neurons receive contacts, as they ascend through L.4 (n=1 brain), but only 30-35 percent of those from L.5 neurons (n=2). Basal dendrites of L.3 neurons also receive few contacts in L.4. This supports the role of layer 4 as an interlaminar relay in association cortex. In addition, our results indicate spatial heterogeneity in the occurrence and number of contacts, possibly due to subtype specificity in target preference. The maximum number of contacts, for a L.2 neuron projecting from anterior to posterior TE, was 29. This approach seems a useful alternative or complement to electron microscopic analyses of long distance connectivity.

Gene expression profiles in two areas of monkey temporal cortex

The frontal association cortex (FrA) is implicated in higher brain function [1]. Aberrant FrA activity is likely to be involved in dementia pathology [2, 3, 4]. However, the functional circuits both within the FrA and with other regions are unclear. A recent study showed that inactivation of the FrA impairs memory consolidation of an auditory fear conditioning in young mice [5]. In addition, dendritic spine remodeling of FrA neurons is sensitive to paired sensory stimuli that produce associative memory [5]. These findings suggest that the FrA is engaged in neural processes critical to associative learning. Here we characterize stimulus integration in the mouse FrA during associative learning. We experimentally separated contextual fear conditioning into context exposure and shock, and found that memory formation requires protein synthesis associated with both context exposure and shock in the FrA. Both context exposure and shock trigger Arc, an activity-dependent immediate-early gene, expression in the FrA, and a subset of FrA neurons was dually activated by both stimuli. In addition, we found that the FrA receives projections from the perirhinal (PRh) and insular (IC) cortices and basolateral amygdala (BLA), which are implicated in context and shock encoding [6, 7, 8]. PRh and IC neurons projecting to the FrA were activated by context exposure and shock, respectively. Arc expression in the FrA associated with context exposure and shock depended on PRh activity and both IC and BLA activities, respectively. These findings indicate that the FrA is engaged in stimulus integration and contributes to memory formation in associative learning.

Visual responses in the temporal cortex to moving objects with invariant contours.

We were interested in how the visual attributes of motion and shape are integrated in the temporal cortex of monkeys. We recorded neural activity in the middle portion of the superior temporal sulcus (STS) of monkeys during a sequential visual discrimination task while the animals maintained fixation. We used images of objects with invariant outlines rotating in 3D space either clockwise or counterclockwise as visual stimuli. In the sequential discrimination task, after the fixation pattern was presented for 1.0 s, the sample stimulus (S1) appeared at the center of the monitor screen for 0.8 s. After a delay period of 0.5-2.0 s, the same stimulus or a new response stimulus appeared on the screen for 0.8 s. In each block, the response stimulus was either a new direction of rotation or a new shape. Of 425 responding neurons isolated in the STS, 202 (48%) showed significant activity when S1 stimuli were presented. Of these visual neurons, 27 (13%) were categorized as motion and shape selective (MS), 69 (34%) as shape selective (S), and 6 (3%) as motion selective (M). Briefer than for MS or S neurons, the latency of the remaining non-selective neurons was 80 ms. Latencies of visual response (110 ms) of both MS and S neurons were similar. On the other hand, MS neurons started responding later (180 ms) to changes in direction. Our findings show that neurons in the STS, responding selectively to changes in shape, do respond to relatively simple motion and that variable contouring is not essential to elicit motion response. The results may also suggest the functional segregation of selective versus non-selective neurons and the later arrival of directional response to MS neurons in the STS.

Textural complexity

The human temporal cortex is known to be involved in visual learning and memory, but its role in visual perception is poorly understood. Studies in macaque monkeys have shown the temporal cortex to have a critical role in complex shape and texture discrimination. Recently, Huxlin and Merigan 1 Huxlin K.R. Merigan W.H. Deficits in complex visual perception following unilateral temporal lobectomy. J. Cogn. Neurosci. 1998; 10: 395-407 Crossref PubMed Scopus (14) Google Scholar tested whether the human temporal cortex is involved in similar tasks by investigating deficits in complex texture- and luminance-based visual discrimination in three patients with temporal lobe lesions. They showed that patient performance (relative to age-matched controls) was specifically affected in tasks involving the perception of texture-based shapes. When shapes were defined by luminance cues, performance was in the normal range or slightly decreased. Interestingly, the discrimination deficits were not restricted to the hemifield contralateral to the lesion site, but occurred equivalently in both visual hemifields. These results are in agreement with data from electrophysiological recordings in monkeys, although the authors emphasize the limited knowledge we have about the homologies between the human and monkey temporal cortex. Finally, it has to be noted that the test of patient performance in object naming based on line drawings did not yield a deficit. This suggests that the temporal lobectomy patients studied in this experiment were impaired only in making subtle visual discriminations, involving complex shapes and/or fine textures. This result is interesting in the light of the localization of the lesions in these patients. Although it is not specifically stated, it seems that their lesions are restricted to the lateral surface of one temporal lobe, mainly in its anterior half. Perhaps this explains the discrepancy between the findings of Huxlin and Merigan in the object naming task and data from visual agnosic patients, whose lesions are usually more ventral and who fail this task. This study proposes that the temporal cortex plays a role in texture-based information processing that may explan its function in specifically complex visual perception.

Consolidation of Visual Associative Long-Term Memory in the Temporal Cortex of Primates

Neuropsychological theories have proposed a critical role for the interaction between the medial temporal lobe and the neocortex in the formation of long-term memory for facts and events, which has often been tested by learning of a series of paired words or figures in humans. We have examined neural mechanisms underlying the memory “consolidation” process by single-unit recording and molecular biological methods in an animal model of a visual pair-association task in monkeys. In our previous studies, we found that long-term associative representations of visual objects are acquired through learning in the neural network of the anterior inferior temporal (IT) cortex. In this article, we propose the hypothesis that limbic neurons undergo rapid modification of synaptic connectivity and provide backward signals that guide the reorganization of neocortical neural circuits. Two experiments tested this hypothesis: (1) we examined the role of the backward connections from the medial temporal lobe to the IT cortex by injecting ibotenic acid into the entorhinal and perirhinal cortices, which provided massive backward projections ipsilaterally to the IT cortex. We found that the limbic lesion disrupted the associative code of the IT neurons between the paired associates, without impairing the visual response to each stimulus. (2) We then tested the first half of this hypothesis by detecting the expression of immediate-early genes in the monkey temporal cortex. We found specific expression ofzif268during the learning of a new set of paired associates in the pair-association task, most intensively in area 36 of the perirhinal cortex. All these results with the visual pair-association task support our hypothesis and demonstrate that the consolidation process, which was first proposed on the basis of clinico-psychological evidence, can now be examined in primates using neurophysiolocical and molecular biological approaches.

Expression of the transcription factor Zif268 in the temporal cortex of monkeys during visual paired associate learning.

In humans and monkeys, memory consists of various components which were initially revealed through neuropsychological studies of amnesic patients. One memory component, the long-term memory about facts and events (declarative memory), has been shown to require the integrity of the medial temporal lobe and the neocortex. To investigate a map of gene expression during declarative memory formation in the primate, we monitored expression of immediate early genes in the temporal lobe of macaque monkeys. We trained the monkeys to learn visual associative memory tasks, and immunohistochemically analysed the expression of protein products of immediate early genes. We found that Zif268, a transcription factor regulated by neuronal activity, accumulated in patches in the anterior temporal lobe during visual stimulus-stimulus association learning, whereas other transcription factors, c-Fos and JunD, were not. By contrast, the patchy expression of Zif268 was not observed during another type of learning, visual discrimination learning. These results suggest that Zif268 activates a gene cascade related to the formation of long-term memory in the primate.