Single cell integration of animate form, motion and location in the superior temporal cortex of the macaque monkey

This study investigated the cellular mechanisms in the anterior part of the superior temporal sulcus (STSa) that underlie the integration of different features of the same visually perceived animate object. Three visual features were systematically manipulated: form, motion and location. In 58% of a population of cells selectively responsive to the sight of a walking agent, the location of the agent significantly influenced the cell's response. The influence of position was often evident in intricate two- and three-way interactions with the factors form and/or motion. For only one of the 31 cells tested, the response could be explained by just a single factor. For all other cells at least two factors, and for half of the cells (52%) all three factors, played a significant role in controlling responses. Our findings support a reformulation of the Ungerleider and Mishkin model, which envisages a subdivision of the visual processing into a ventral 'what' and a dorsal 'where' stream. We demonstrated that at least part of the temporal cortex ('what' stream) makes ample use of visual spatial information. Our findings open up the prospect of a much more elaborate integration of visual properties of animate objects at the single cell level. Such integration may support the comprehension of animals and their actions.     

Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex

The responses of neurons in the middle temporal and medial superior temporal areas of macaque cortex are suppressed during saccades compared with saccade-like stimulus movements. We utilized the short-latency ocular following paradigm to show that this saccadic suppression is followed by postsaccadic enhancement of motion responses. The level of enhancement decays with a time constant of 100 ms from saccade end. The speed of ocular following is also enhanced after saccades and decays over a similar time course, suggesting a link between the neural and behavioral effects. There is some evidence that maximum postsaccadic enhancement occurs when cells are stimulated at their optimum speeds. Latencies of motion responses are saccade dependent: 37 ms for saccade-generated motion, 45 ms for motion in the half-second after saccades, and 70 ms with no prior saccades. The finding that saccades alter response latencies may partially explain perceptual time compression during saccades and time dilation after saccades.     

Organization of horizontal axons in the inferior temporal cortex and primary visual cortex of the macaque monkey

We investigated the organization of horizontal connections at two distinct hierarchical levels in the ventral visual cortical pathway of the monkey, the inferior temporal (TE) and primary visual (V1) cortices. After injections of anterograde tracers into layers 2 and 3, clusters of terminals ('patches') of labeled horizontal collaterals in TE appeared at various distances up to 8 mm from the injection site, while in V1 clear patches were distributed only within 2 mm. The size and spacing of these patches in TE were larger and more irregular than those observed in V1. The labeling intensity of patches in V1 declined sharply with distance from the injection site. This tendency was less obvious in TE; a number of densely labeled patches existed at distant sites beyond weakly labeled patches. While injections into both areas resulted in an elongated pattern of patches, the anisotropy was greater in TE than in V1 for injections of a similar size. Dual tracer injections and larger-sized injections further revealed that the adjacent sites in TE had spatially distinct horizontal projections, compared to those in V1. These area-specific characteristics of the horizontal connections may contribute to the differences in visual information processing of TE and V1.     

A stable topography of selectivity for unfamiliar shape classes in monkey inferior temporal cortex

The inferior temporal (IT) cortex in monkeys plays a central role in visual object recognition and learning. Previous studies have observed patches in IT cortex with strong selectivity for highly familiar object classes (e.g., faces), but the principles behind this functional organization are largely unknown due to the many properties that distinguish different object classes. To unconfound shape from meaning and memory, we scanned monkeys with functional magnetic resonance imaging while they viewed classes of initially novel objects. Our data revealed a topography of selectivity for these novel object classes across IT cortex. We found that this selectivity topography was highly reproducible and remarkably stable across a 3-month interval during which monkeys were extensively trained to discriminate among exemplars within one of the object classes. Furthermore, this selectivity topography was largely unaffected by changes in behavioral task and object retinal position, both of which preserve shape. In contrast, it was strongly influenced by changes in object shape. The topography was partially related to, but not explained by, the previously described pattern of face selectivity. Together, these results suggest that IT cortex contains a large-scale map of shape that is largely independent of meaning, familiarity, and behavioral task.     

Three-dimensional structure-from-motion selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey

Human and non-human primates are able to perceive three-dimensional structure from motion displays. Three-dimensional structure-from-motion (object-motion) displays were used to test the hypothesis that neurons in the anterior division of the superior temporal polysensory area (STPa) of monkeys can selectively respond to three-dimensional structure-from-motion. Monkeys performed a reaction time task that required the detection of a change in the fraction of structure in three-dimensional transparent sphere displays. Neurons were able to distinguish structured and unstructured three-dimensional optic flow. These cells could differentiate the change in structure-from-motion at stimulus presentation and when the animal was detecting the amount of structure in the display. Some of these neurons were also tuned for characteristics of the sphere stimuli. Cells were also tested with navigational motion and many were found to respond both to three-dimensional structure-from-motion and navigational motion. These results suggest that STPa neurons represent specific aspects of three-dimensional surface structure and that neurons within STPa contribute to the perception of three-dimensional structure-from-motion.     

Neural bases of stereopsis across visual field of the alert macaque monkey

Left and right retinal images of an object seen by the 2 eyes can occupy slightly disparate horizontal and/or vertical locations. The role of horizontal disparity (HD) in stereoscopic vision is well established, but the functional contribution of vertical disparity (VD) remains unclear. Various psychophysical studies have shown that HD and VD are used differently by the visual system depending on their location in the visual field, whether near the center of gaze or more peripheral. We show this horizontal/vertical distinction at the cellular level in monkey primary visual cortex (area V1). The range of VD encoding is reduced in central but not in the peripheral representation of the visual field. Moreover, neurons respond selectively to particular combinations of both types of disparities depending on the coded orientation as predicted by the disparity energy model. The preferred orientations of neurons near the fovea present a vertical bias that is well suited for stereopsis based on HD selectivity alone. In the periphery, instead, preferred orientations are radially biased, which allows a peripheral detector to convey the same depth signal based on either HD or VD. Such an organization has functional implications in both the perceptual and oculomotor domains.     

The pyramidal cell of the sensorimotor cortex of the macaque monkey: phenotypic variation

Recent studies have revealed striking differences in pyramidal cell structure among cortical regions involved in the processing of different functional modalities. For example, cells involved in visual processing show systematic variation, increasing in morphological complexity with rostral progression from V1 through extrastriate areas. Differences have also been identified between pyramidal cells in somatosensory, motor and prefrontal cortex, but the extent to which the pyramidal cell phenotype may vary between these functionally related cortical regions remains unknown. In the present study we investigated the structure of layer III pyramidal cells in somatosensory and motor areas 3b, 4, 5, 6 and 7b of the macaque monkey. Cells were intracellularly injected in fixed, flat-mounted cortical slices and analysed for morphometric parameters. The size of the basal dendritic arbours, the number of their branches and their spine density were found to vary systematically between areas. Namely, we found a trend for increasing complexity in dendritic arbour structure through areas 3b, 5 and 7b. A similar trend occurred through areas 4 and 6. The differences in arbour structure may determine the number of inputs received by neurons and may thus be an important factor in determining function at the cellular and systems level.     

The anatomical connections of the macaque monkey orbitofrontal cortex. A review

The orbitofrontal cortex (OfC) is a heterogeneous prefrontal sector selectively connected with a wide constellation of other prefrontal, limbic, sensory and premotor areas. Among the limbic cortical connections, the ones with the hippocampus and parahippocampal cortex are particularly salient. Sensory cortices connected with the OfC include areas involved in olfactory, gustatory, somatosensory, auditory and visual processing. Subcortical structures with prominent OfC connections include the amygdala, numerous thalamic nuclei, the striatum, hypothalamus, periaqueductal gray matter, and biochemically specific cell groups in the basal forebrain and brainstem. Architectonic and connectional evidence supports parcellation of the OfC. The rostrally placed isocortical sector is mainly connected with isocortical areas, including sensory areas of the auditory, somatic and visual modalities, whereas the caudal non-isocortical sector is principally connected with non-isocortical areas, and, in the sensory domain, with olfactory and gustatory areas. The connections of the isocortical and non-isocortical orbital sectors with the amygdala, thalamus, striatum, hypothalamus and periaqueductal gray matter are also specific. The medial sector of the OfC is selectively connected with the hippocampus, posterior parahippocampal cortex, posterior cingulate and retrosplenial areas, and area prostriata, while the lateral orbitofrontal sector is the most heavily connected with sensory areas of the gustatory, somatic and visual modalities, with premotor regions, and with the amygdala.     

Beyond superior temporal cortex: intersubject correlations in narrative speech comprehension

The role of superior temporal cortex in speech comprehension is well established, but the complete network of regions involved in understanding language in ecologically valid contexts is less clearly understood. In a functional magnetic resonance imaging (fMRI) study, we presented 24 subjects with auditory or audiovisual narratives, and used model-free intersubject correlational analyses to reveal brain areas that were modulated in a consistent way across subjects during the narratives. Conventional comparisons to a resting state were also performed. Both analyses showed the expected recruitment of superior temporal areas, however, the intersubject correlational analyses also revealed an extended network of areas involved in narrative speech comprehension. Two findings stand out in particular. Firstly, many areas in the "default mode" network (typically deactivated relative to rest) were systematically modulated by the time-varying properties of the auditory or audiovisual input. These areas included the anterior cingulate and adjacent medial frontal cortex, and the posterior cingulate and adjacent precuneus. Secondly, extensive bilateral inferior frontal and premotor regions were implicated in auditory as well as audiovisual language comprehension. This extended network of regions may be important for higher-level linguistic processes, and interfaces with extralinguistic cognitive, affective, and interpersonal systems.     

A study of pyramidal cell structure in the cingulate cortex of the macaque monkey with comparative notes on inferotemporal and primary visual cortex

Recent studies have revealed a marked degree of variation in the pyramidal cell phenotype in visual, somatosensory, motor and prefrontal cortical areas in the brain of different primates, which are believed to subserve specialized cortical function. In the present study we carried out comparisons of dendritic structure of layer III pyramidal cells in the anterior and posterior cingulate cortex and compared their structure with those sampled from inferotemporal cortex (IT) and the primary visual area (V1) in macaque monkeys. Cells were injected with Lucifer Yellow in flat-mounted cortical slices, and processed for a light-stable DAB reaction product. Size, branching pattern, and spine density of basal dendritic arbors was determined, and somal areas measured. We found that pyramidal cells in anterior cingulate cortex were more branched and more spinous than those in posterior cingulate cortex, and cells in both anterior and posterior cingulate were considerably larger, more branched, and more spinous than those in area V1. These data show that pyramidal cell structure differs between posterior dysgranular and anterior granular cingulate cortex, and that pyramidal neurons in cingulate cortex have different structure to those in many other cortical areas. These results provide further evidence for a parallel between structural and functional specialization in cortex.     

Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex

Whereas much is known about the visual shape selectivity of neurons in the inferior temporal cortex (ITC), less is known about the role of visual learning in the development and refinement of ITC shape selectivity. To address this, we trained monkeys to perform a visual categorization task with a parametric set of highly familiar stimuli. During training, the stimuli were always presented at the same orientation. In this experiment, we recorded from ITC neurons while monkeys viewed the trained stimuli in addition to image-plane rotated versions of those stimuli. We found that, concomitant with the monkeys' behavioral performance, neuronal stimulus selectivity was stronger for stimuli presented at the trained orientation than for rotated versions of the same stimuli. We also recorded from ITC neurons while monkeys viewed sets of novel and familiar (but not explicitly trained) randomly chosen complex stimuli. We again found that ITC stimulus selectivity was sharper for familiar than novel stimuli, suggesting that enhanced shape tuning in ITC can arise for both passively experienced and explicitly trained stimuli.     

Role of the superior temporal region in human visual motion perception

While moving objects are usually seen using luminance (first-order) cues, humans can perceive the motion of objects via non-luminance (second-order) cues. Contrary to previous case reports, no physiological studies have elucidated distinct differences in the cortical regions involved in first- and second-order motion processes. We investigated brain responses related to these two types of motion perception in human subjects using 3 T functional magnetic resonance imaging and strictly controlled apparent motion stimulus pairs. Comparison of brain activation to moving versus static states of each motion stimulus isolated cortical activity related to each type of motion perception. We found a selective neural response to second-order motion stimulus in the anterior part of the superior temporal sulcus (STS) contralateral to stimulus presentation and cue-invariant activation of MT/V5+. No significant activation in the STS was observed by the first-order motion, even when its visibility was reduced to levels comparable to that of second-order motion. Furthermore, the STS demonstrated significant activation for highly visible motion stimulus with both first- and second-order attributes. The STS represents the cardinal structure for perception of second-order motions, although further studies are needed to elucidate the exact neural process occurring in this area.     

Functional organization of temporal frequency selectivity in primate visual cortex

Several studies have shown that neurons with similar response properties are arranged together in domains across primary visual cortex (V1). An orderly pattern of domains has been described for preferences to ocular dominance, orientation, and spatial frequency. Temporal frequency preference, another important attribute of the visual scene, also might be expected to map into different domains. Using optical imaging and a variety of quantitative methods, we examined how temporal frequency selectivity is mapped in V1 of the prosimian primate, bush baby (Otolemur garnetti). We found that unlike other attribute maps, selectivity for different temporal frequencies is arranged uniformly across V1 with no evidence of local clustering. Global tuning for temporal frequency, based on magnitude of response, showed a good match to previous tuning curves for single neurons. A peak response was found around 2.0 Hz, with smaller attenuation at lower temporal frequencies than at higher frequencies. We also examined whether the peak temporal frequency response differed between anatomical compartments defined by cytochrome oxidase (CO). No significant differences in the preference for temporal frequency were found between these CO compartments. Our findings show that key sensory attributes that are linked in perception can be organized in quite distinct ways in V1 of primates.     

Inhibitory synapse cover on the somata of excitatory neurons in macaque monkey visual cortex

Electron microscopy was used in macaque monkey cortical area V1 to investigate what factors might determine the proportion of somatic membrane covered by inhibitory type 2 synapses. In a sample of 4654 excitatory neurons, synapse cover did not correlate consistently with cell variety (pyramid or spiny stellate), soma size, synaptic apposition length or thalamic input. There were significant differences in somatic synapse cover per layer, but the pattern of differences in cover among layers differed significantly between animals, suggesting that laminar environment alone is not a generally applicable determinant of amount of inhibitory synapse cover. The pattern of cover for cells in different layers was, however, similar between the two hemispheres of an individual monkey. Measures of inhibitory synapse cover on four sets of pyramidal neurons in layers 5 and 6, each with different efferent projection targets, showed that the sets differed significantly from other cells in their respective layers, and differed significantly from each other. These findings demonstrate that there is unique circuitry for different subsystems within single layers of cortex and provide a rationale for the rich variety of cortical GABAergic interneurons within single layers.     

Reciprocal connectivity of identified color-processing modules in the monkey inferior temporal cortex

The inferior temporal (IT) cortex is the last unimodal visual area in the ventral visual pathway and is essential for color discrimination. Recent imaging and electrophysiological studies have revealed the presence of several distinct patches of color-selective cells in the anterior IT cortex (AIT) and posterior IT cortex (PIT). To understand the neural machinery for color processing in the IT cortex, in the present study, we combined anatomical tracing methods with electrophysiological unit recordings to investigate the anatomical connections of identified clusters of color-selective cells in monkey IT cortex. We found that a color cluster in AIT received projections from a color cluster in PIT as well as from discrete clusters of cells in other occipitotemporal areas, in the superior temporal sulcus, and in prefrontal and parietal cortices. The distribution of the labeled cells in PIT closely corresponded with that of the physiologically identified color-selective cells in this region. Furthermore, retrograde tracer injections in the posterior color cluster resulted in labeled cells in the anterior cluster. Thus, temporal lobe color-processing modules form a reciprocally interconnected loop within a distributed network.     

Cell type- and region-specific expression of neurogranin mRNA in the cerebral cortex of the macaque monkey

Neurogranin is a postsynaptic substrate for protein kinase C (PKC). It has been identified in the central nervous system, and the expression has been related to postsynaptic plasticity. Using non-radioactive in situ hybridization histochemistry, we investigated whether mRNA expression of neurogranin varied among the cerebral region and cell types. In most areas of the neocortex excluding area OC (the primary visual area), intense signals were observed in the pyramidal cells in layers III, V and VI. In area OC, intense signals were observed in layers IV as well as layers III and VI. We previously showed that intense signals for GAP-43, a presynaptic PKC substrate, were observed in relay neurons of the lateral geniculate nucleus. From this result and the present result in area OC, we conclude that both pre- and postsynaptic PKC substrates (GAP-43 and neurogranin) are abundant in the geniculocortical synapses. In the hippocampus, intense signals were observed in the pyramidal cells in the subiculum. Taken together with our previous study showing intense signals for GAP-43 in Ammon's horn, the result indicates that both PKC substrates are abundant in the connections between neurons in Ammon's horn and in the subiculum.     

Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex

We compared the morphological characteristics of layer III pyramidal neurones in different visual areas of the occipitotemporal cortical 'stream', which processes information related to object recognition in the visual field (including shape, colour and texture). Pyramidal cells were intracellularly injected with Lucifer Yellow in cortical slices cut tangential to the cortical layers, allowing quantitative comparisons of dendritic field morphology, spine density and cell body size between the blobs and interblobs of the primary visual area (V1), the interstripe compartments of the second visual area (V2), the fourth visual area (V4) and cytoarchitectonic area TEO. We found that the tangential dimension of basal dendritic fields of layer III pyramidal neurones increases from caudal to rostral visual areas in the occipitotemporal pathway, such that TEO cells have, on average, dendritic fields spanning an area 5-6 times larger than V1 cells. In addition, the data indicate that V1 cells located within blobs have significantly larger dendritic fields than those of interblob cells. Sholl analysis of dendritic fields demonstrated that pyramidal cells in V4 and TEO are more complex (i.e. exhibit a larger number of branches at comparable distances from the cell body) than cells in V1 or V2. Moreover, this analysis demonstrated that the dendrites of many cells in V1 cluster along specific axes, while this tendency is less marked in extrastriate areas. Most notably, there is a relatively large proportion of neurones with 'morphologically orientation-biased' dendritic fields (i.e. branches tend to cluster along two diametrically opposed directions from the cell body) in the interblobs in V1, as compared with the blobs in V1 and extrastriate areas. Finally, counts of dendritic spines along the length of basal dendrites revealed similar peak spine densities in the blobs and the interblobs of V1 and in the V2 interstripes, but markedly higher spine densities in V4 and TEO. Estimates of the number of dendritic spines on the basal dendritic fields of layer III pyramidal cells indicate that cells in V2 have on average twice as many spines as V1 cells, that V4 cells have 3.8 times as many spines as V1 cells, and that TEO cells have 7.5 times as many spines as V1 cells. These findings suggest the possibility that the complex response properties of neurones in rostral stations in the occipitotemporal pathway may, in part, be attributed to their larger and more complex basal dendritic fields, and to the increase in both number and density of spines on their basal dendrites.      

Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey

The prefrontal cortex selects relevant signals and suppresses irrelevant signals in behavior, as exemplified by its functional interaction with superior temporal cortices. We addressed the structural basis of this process by investigating quantitatively the relationship of prefrontal pathways to inhibitory interneurons in superior temporal cortices. Pathways were labeled with neural tracers, and two neurochemical classes of inhibitory interneurons were labeled with parvalbumin (PV) and calbindin (CB), which differ in mode of inhibitory control. Both markers varied significantly and systematically across superior temporal areas. Calbindin neurons were more prevalent than PV neurons, with the highest densities found in posterior high-order auditory association cortices. Axons from anterior lateral, medial prefrontal and orbitofrontal areas terminated in the anterior half of the superior temporal gyrus, targeting mostly the superficial layers (I to upper III), where CB neurons predominated. Reciprocal projection neurons were intermingled with PV neurons, and emanated mostly from the deep part of layer III and to a lesser extent from layers V-VI, in proportions matching the laminar density of inhibitory interneurons. In marked contrast, prefrontal connections in temporal polar cortex were found mostly in the deep layers, showing mismatch with the predominant upper laminar distribution of interneurons. Differences in the relationship of connections to inhibitory neurons probably affect the dynamics in distinct superior temporal cortices. These findings may help explain the reduced efficacy of inhibitory control in superior temporal areas after prefrontal cortical damage.     

Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: An electrophysiological study in the macaque monkey

To elucidate the functions of nonprimary motor cortical (nPMC) areas whose afferents synapse onto output neurons of the primary motor cortex (PMC), we examined the responses of pyramidal tract neurons (PTNs) and non-PTNs (nPTNs) to electrical stimulation in the three nPMCs, the supplementary motor area (SMA) and the dorsal and ventral divisions of the premotor cortex (PMd and PMv), with extracellular unit recording in alert monkeys. Typical responses of PTNs to nPMC stimulation were early orthodromic excitatory responses followed by inhibitory responses. Among 27 PTNs tested by constructing peri-stimulus time histograms, 19 (70.4%) showed inhibitory responses to stimulation in all of the nPMC areas. In contrast, 5/33 PTNs (15.2%) and 10/72 nPTNs (13.9%) showed excitatory responses to stimulation in all of the nPMCs. The inhibitory responses of PTNs were mediated by inhibitory interneurons, some of which may correspond to nPTNs in the superficial layers of the PMC. These interneurons probably possess widely extended axons and nonspecifically inhibit multiple PTNs in layer V. The excitatory and inhibitory influences, and the patterns of convergence of inputs from the nPMCs onto the PTNs, are important to understand motor control by the nPMC-PMC-spinal cord pathway.     

Effects of illumination intensity and direction on object coding in macaque inferior temporal cortex

Single unit activity in area TE was recorded from two macaques as they viewed 3D appearing rendered objects that were illuminated from different directions (without cast shadows) and intensities of illumination. The average modulation produced by changes in illumination intensity or direction was rather moderate, with the majority of the neurons responding invariantly to these lighting variables. When neural activity was affected by illumination direction, it was not manifested as a preference for a particular direction of illumination by a given neuron. Instead, the tuning appeared to be to the relative brightness of a given shaped surface at a given orientation. The modulation to changes in illumination direction was considerably smaller than that produced by changes in object shape. Most of the neurons that were unaffected by changes in illumination direction responded much less to silhouettes of these objects, indicating that these neurons were also sensitive to an object's inner features. The neuronal invariance for shading variations may provide the basis for the invariance of object recognition under changes in illumination.