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In primates, prefrontal, inferior temporal, and posterior parietal cortex are important for cognitive function. It is shown that in adult macaques, new neurons are added to these three neocortical association areas, but not to a primary sensory area (striate cortex). The new neurons appeared to originate in the subventricular zone and to migrate through the white matter to the neocortex, where they extended axons. These new neurons, which are continually added in adulthood, may play a role in the functions of association neocortex.

We previously found [42] that lesions of the superior temporal polysensory area (STP) cause temporary deficits in the production of eye movements. In order to both define regions participating in the ensuing recovery and to further explore the cortical control of eye movements, we examined the effects of addition of frontal eye field (FEF) lesions to STP lesions, on visual fixation, saccadic eye movements, and smooth pursuit eye movements. Three monkeys received bilateral STP lesions followed by a FEF lesion and as a control, an additional monkey received a bilateral inferior temporal cortex (IT) lesion followed by a FEF lesion. All animals had a profound impairment in foveating the central fixation point. This impairment was completely eliminated by turning on a dim light in the testing chamber. Large neglect-like impairments in making saccades were only seen after combined STP and FEF lesions. Impairments in making smooth pursuit eye movements after combined lesions of STP and FEF were larger than those seen after STP lesions but within the range of deficits that have been reported after FEF lesions alone. The impairment of visual fixation in darkness and the lack of impairment under conditions of dim illumination appear to reflect a specific role for the FEF in spatial orientation in the absence of visual landmarks. The FEF also appears to play a more critical role than STP in smooth pursuit. By contrast, STP and the FEF appear to work cooperatively with respect to the production of saccades. We suggest that cortical oculomotor control can flow either through the midbrain or through the FEF and that the FEF pathway is specifically involved in tasks with a discontiguity between the stimuli and the behavioral response while the midbrain pathways are preferentially involved in more stimulus-driven eye movements.

Three monkeys with extensive preoperative training on visual and auditory memory tasks (delayed matching-to-sample), an auditory pattern-discrimination task, and a visual serial-order task, received bilateral lesions of the superior temporal (ST) cortex in two stages, with testing after each lesion. Unilateral ST cortex lesions resulted in only moderate auditory memory impairments, whereas bilateral ST cortex lesions resulted in severe auditory memory impairments. The bilateral ST cortex lesions also resulted in severe impairments in the ability to relearn the auditory pattern-discrimination task. In contrast to the auditory impairments, neither unilateral nor bilateral ST cortex lesions had any effect whatsoever on either visual memory or visual serial-order behavior. These findings indicate that the ST cortex plays a role in auditory processing and retention similar to that played by the inferior temporal cortex for visual processing and retention.

1. On the basis of its anatomic connections and single-unit properties, the superior temporal polysensory area (STP) would seem to be primarily involved in visuospatial functions. We have examined the effects of lesions of STP on saccadic eye movements, visual fixation, and smooth pursuit eye movements to directly test the hypothesis that STP is involved in visuospatial and visuomotor behavior. 2. Seven monkeys were trained to make saccades to targets 8, 15, and 22 degrees from a central fixation point along the horizontal meridian and 8 degrees from the central fixation point along the vertical meridian. One monkey was also trained to make saccades to auditory targets. The same monkeys were trained to foveate a stationary central fixation point and to follow it with a smooth pursuit eye movement when it began moving 5, 13, or 20 degrees/s. Four monkeys received unilateral STP lesions, one received a bilateral STP lesion, and as a control, two received unilateral inferior temporal cortex (IT) lesions. After testing, three of the animals with unilateral STP lesions received an additional STP lesion in the hemisphere contralateral to the first lesion. Similarly, one animal with a unilateral IT lesion received an additional IT lesion in the hemisphere contralateral to the first lesion. 3. All monkeys with complete removal of STP showed a significant increase in saccade latency to the most peripheral contralateral target, and most also had increased saccade latencies to the other contralateral targets. Saccades directed to targets along the vertical meridian or toward targets in the hemifield ipsilateral to the lesion were not impaired by removal of STP. By contrast, IT lesions did not impair the monkeys' ability to make saccadic eye movements to visual stimuli at any location, showing that saccades to visually guided targets are not impaired nonspecifically by damage to visual cortex. 4. The deficit in making eye movements after STP lesions was specific to saccade latency, with little effect on the accuracy of saccades to visual targets. 5. In the one monkey trained to make saccades to auditory targets, removal of STP did not impair saccades to auditory targets contralateral to its lesion, despite this monkey showing the largest increase in saccades latencies to visual targets. 6. There was complete recovery of saccade latency to the baseline level of performance on the saccade task after all STP lesions.(ABSTRACT TRUNCATED AT 400 WORDS)

The origins of contemporary work on the temporal cortex and object recognition are traced from their roots in phrenology through the search for a cortical visual area to the discovery of the Klüver-Bucy syndrome and its fractionation, finally ending with early single-neuron recording studies.

Single-unit activity was recorded from inferior temporal (IT) cortex and the hippocampus in 2 macaques trained on auditory-visual and visual-visual delayed matching-to-sample tasks. The main purpose of the study was to compare the response properties of delay neurons between the 2 areas. The authors noted that (a) IT cortex delay activity was usually selective to a particular stimulus, whereas hippocampal delay activity was usually nonselective; (b) the level of delay activity was generally larger in the hippocampus than in IT cortex; and (c) unlike IT cortex delay activity, hippocampal delay activity tended to increase in magnitude as the delay progressed. The authors also examined the functional significance of delay activity and noted a higher probability of encountering a delay neuron when the monkeys were performing 75%-100% correct as compared with 50%-75% correct. The significance of these findings for visual recognition memory is discussed.

1. Isolated, single-neuron extracellular potentials were recorded sequentially in area TE of the inferior temporal cortex (IT) of two macaque monkeys (n = 58 and n = 41 neurons). Data were obtained while the animals were performing a paired-associate task. The task utilized five stimuli and eight stimulus pairings (4 correct and 4 incorrect). Data were evaluated as average spike rate during experimental epochs of 100 or 400 ms. Single-unit and population characteristics were measured using a form of linear discriminant analysis and information theoretic measures. To evaluate the significance of covariance on population code measures, additional data consisting of simultaneous recordings from < or = 8 isolated neurons (n = 37) were obtained from a third macaque monkey that was passively viewing visual stimuli. 2. On average, 43% of IT neurons were activated by any of the stimuli used (60% if those inhibited also are included). Yet the neurons were rather unique in the relative magnitude of their responses to each stimulus in the test set. These results suggest that information may be represented in IT by the pattern of activity across neurons and that the representation is not sparsely coded. It is further suggested that the representation scheme may have similarities to DNA or computer codes wherein a coding element is not a local parametric descriptor. This is a departure from the V1 representation, which appears to be both local and parametric. It is also different from theories of IT representation that suggest a constructive basis set or "alphabet". From this view, determination of stimulus discrimination capacity in IT should be evaluated by measures of population activity patterns. 3. Evaluation of small groups of simultaneously recorded neurons obtained during a fixation task suggests that little information about visual stimuli is conveyed by covariance of activity in IT when a 100-ms time scale is used as in this study. This finding is consistent with a prior report, by Gochin et al., which used a 1-ms time scale and failed to find neural activity coherence or oscillations dependent on stimuli. 4. Population-stimulus-discrimination capacity measures were influenced by the number of neurons and to some extent the number and type of stimuli. 5. Information conveyed by individual neurons (mutual information) averaged 0.26 bits. The distribution of information values was unimodal and is therefore more consistent with a distributed than a local coding scheme.(ABSTRACT TRUNCATED AT 400 WORDS)

Four monkeys were trained preoperatively on a serial-order task to respond to a set of five visual stimuli in a fixed sequence independent of their location. They were then given a test of visual imagery in which only two of the five stimuli appeared at a time, and the animals were required to respond to them in the order in which they appeared in the original sequence. The monkeys then received bilateral lesions of either inferior temporal cortex or dorsolateral frontal cortex. Dorsolateral frontal lesions had no effect on either serial-order behavior or visual imagery. In contrast, inferior temporal lesions severely impaired serial-order behavior. Once the serial-order task was relearned, however, the inferior temporal animals were completely normal on the test of visual imagery.

1. Inferior temporal cortex (IT) is a "high-order" region of primate temporal visual cortex implicated in visual pattern perception and recognition. To gain some insight into the development of this area, we compared the properties of single neurons in IT in infant monkeys ranging from 5 wk to 7 mo of age with those of neurons in IT in adult animals. Both anesthetized and awake behaving paradigms were used. 2. In immobilized infant monkeys under nitrous oxide anesthesia, the incidence of visually responsive cells was markedly less than in adult monkeys studied under similar conditions. In infants 4-7 mo of age, only half of IT neurons studied were visually responsive, compared with > 80% in adult monkeys. In monkeys < 4 mo old, even fewer (< 10%) could be visually driven. "Habituation" of IT cells to repeated stimulus presentation appeared more pronounced in infant monkeys under nitrous oxide anesthesia than in adult animals. 3. IT cells in the anesthetized infant monkeys that did respond showed receptive field properties similar to those of responsive adult IT neurons studied under similar conditions. Two thirds of the receptive fields plotted in the anesthetized 4 to 7-mo-old group were bilateral, and median field size did not differ between the infants and comparable adult groups, being approximately 20 degrees on a side in each case. 4. In contrast to the results obtained under anesthesia, most IT cells in alert infant monkeys 5 wk-7 mo of age (80%) were responsive to visual stimuli, and this incidence of visually responsive IT neurons did not differ from that obtained in awake adult macaques. However, response magnitude, measured as spikes per second above baseline rate, was significantly lower in the infant alert sample than in the adult control (5.2 vs. 12.6 spikes/s, mean +/- SE, deviation from spontaneous rate, respectively). 5. In addition to having lower magnitudes of visual response, IT cells in the awake infants also tended to have longer and more variable latencies. The overall mean for the infant cells was 196 ms, compared with an overall mean of 140 ms for IT neurons in the alert control adult. 6. Although the magnitude of response of neurons in alert infant IT cortex was lower overall, the incidence and features of stimulus selectivity shown by alert infant IT neurons were strikingly similar to those of IT cells of both anesthetized and unanesthetized adult monkeys.(ABSTRACT TRUNCATED AT 400 WORDS)

The responses of neurons, in inferior temporal cortex of the awake macaque, to single stimuli and pairs of stimuli were examined. The responses of most neurons were weaker to pairs of stimuli than to the best single stimulus of that pair presented alone. This 'suppression by a second stimulus' did not appear to be stimulus-selective and the suppression was greater when the second stimulus appeared in receptive field locations that exhibited weaker responses. This phenomenon suggests competitive interactions between IT neurons that may be involved in visual attention or learning or both.

Six rhesus monkeys took part in an experiment on visual learning. In three of the monkeys the part of the superior temporal sulcus in which many of the cells respond selectively to some aspect of faces was removed, while the remaining three animals served as unoperated controls. In Experiment 1 they learned a series of two-choice visual discriminations between patterns. The animals with lesions of the superior temporal sulcus were markedly impaired. The discriminations were of two types: in the first, the discriminanda differed in shape (e.g. Y and 3), while in the second they differed only in their orientation (e.g. ). Unlike animals with lesions to the neighbouring inferior temporal cortex who are impaired on shape but not orientation discriminations, animals with lesions of the superior temporal sulcus were equally impaired on both types of discrimination. In Experiment 2 the same six animals learned a series of discriminations between discriminanda which consisted of photographs of pairs of eyes. Each discrimination was between a set of eyes which looked directly at the viewer and a set in which the gaze was laterally averted to varying degrees. Again, animals with lesions of the superior temporal sulcus showed a marked impairment. We conclude that this impairment may be a general impairment in two-choice visual discrimination learning, rather than a selective impairment in discrimination of eye gaze. This result warns against a simple interpretation of the function of this area as a "face area", concerned only, or chiefly, with the perception and significance of parts of the body, notably faces, and their movements.

In primates, inferior temporal (IT) cortex is crucial for the processing and storage of visual information about form and colour. This article reviews the properties of IT neurons and considers how these properties may underlie the perceptual and mnemonic functions of IT cortex. The available evidence suggests that the processing of the facial image by IT cortex is similar to its processing of other visual patterns. Faces and other complex visual stimuli appear to be represented by the pattern of responses over a population of IT neurons rather than by the responses of specific 'feature detectors' or 'grandmother' cells. IT neurons with adult-like stimulus properties are present in monkeys as young as six weeks old.

Inferior temporal cortex is necessary for visual object recognition in adult primates but is less critical in infants. Nonetheless, in macaques as young as 6 weeks old, inferior temporal neurons showed adult-like visual response properties, including form selectivity and bilateral receptive fields, indicating that extended maturation and visual experience may not be necessary for adult-like encoding of complex objects. However, before the animals were 4 months old, visual responsiveness was found in inferior temporal cortex only in awake monkeys performing a behavioral task and not in anesthetized ones, suggesting that extraretinal factors profoundly influence function in "association" cortex in developing as well as mature animals.

We studied the visual responses of single neurons in three extra-striate visual areas of the macaque following lesions of striate cortex, lesions of the tecto-pulvinar system or both. After striate lesions, there was (a) considerable specific activity remaining in area MT including direction selectivity, (b) only non-specific activity in the superior temporal polysensory area (STP), and (c) no visual responsiveness at all in inferior temporal cortex (IT). In animals with striate lesions, interruption of the tecto-pulvinar pathway eliminated the residual visual activity in MT and STP that survived the striate lesions. Interruption of the tecto-pulvinar pathway alone had little or no effect on visual evoked activity in any of the three areas. These results are related to the relative dependence of visual responsiveness in MT, STP and IT on striate cortex and the superior colliculus, to differences between the dorsal and ventral cortical processing streams, and to neural mechanisms underlying blind sight.

Functional interactions among inferior temporal cortex (IT) neurons were studied in the awake, fixating macaque monkey during the presentation of visual stimuli. Extracellular recordings were obtained simultaneously from several microelectrodes, and in many cases, spike trains from more than one neuron were extracted from each electrode by the use of spike shape sorting technology. Functional interactions between pairs of neurons were measured using cross-correlation. Discharge patterns of single neurons were evaluated using auto-correlation and PST histograms. Neurons recorded on the same electrode (within about 100 microns) had more similar stimulus selectivity and were more likely to show functional interactions than those recorded on different electrodes spaced about 250 to 500 microns apart. Most neurons tended to fire in bursts tens to hundreds of milliseconds in duration, and asynchronously from the stimulus induced rate changes. Correlated neuronal firing indicative of shared inputs and direct interactions was observed. Occurrence of shared input was significantly lower for neuron pairs recorded on different electrodes than for neurons recorded on the same electrode. Direct connections occurred about as often for neurons on different electrodes as for neurons on the same electrode. These results suggest that input projections are usually restricted to less than 500 micron patches and are then distributed over greater distances by intrinsic connections. Measurements of synaptic contribution suggest that typically more than 5 near-simultaneous inputs are required to cause an IT neuron to discharge.

Monkeys with inferior temporal (IT) cortex lesions were compared with normal and operated control monkeys on a series of two-choice visual discrimination problems. In some problems, the discriminanda were different patterns or objects whereas, in other problems, the discriminanda were identical patterns or objects presented in different orientations. The animals with IT lesions were significantly impaired in learning to discriminate the different patterns and objects; however, they were not impaired in learning to discriminate stimuli which differed only in orientation by 60 degrees or more. These results help to specify further the role of the IT cortex in visual associative learning by demonstrating that there are some types of visual discriminations which are not sensitive to IT lesions.

Visual receptive fields and responsiveness of neurons to somesthetic and auditory stimuli were studied in the inferior temporal cortex and adjacent regions of immobilized macaques. Neurons throughout cytoarchitectonic area TE were responsive only to visual stimuli and had large receptive fields that almost always included the center of gaze and usually extended into both visual half-fields. There was no indication of any visuotopic organization within area TE. Neurons in an anterior and in a dorsal portion of TE tended to have larger receptive fields. By contrast, dorsal, ventral and anterior to area TE, units often responded to somesthetic and auditory as well as to visual stimuli. In these regions visual receptive fields were even larger than in TE and often included the entire visual field. Posterior to TE the neurons were exclusively visual and had much smaller receptive fields that were confined to the contralateral visual field and were topographically organized.

Neurons in inferior temporal cortex of the rhesus monkey usually have large receptive fields that extend well across the midline into both visual half-fields. The responsiveness of these neurons to stimuli in the ipsilateral visual half-field depends on the splenium and anterior commissure, the same pathways necessary for interhemispheric transfer of visual habits. Since inferior temporal neurons have the same trigger features in both half-fields and are usually binocular, they may be the site of the interhemispheric neural convergence that underlies interhemispheric transfer. If so, bilateral removal of inferior temporal cortex should interfere with interhemispheric transfer even when the commissures are intact. To test this, monkeys were trained on pattern discriminations with one eye and then tested for transfer with the other eye. Five experimental monkeys received bilateral inferior temporal lesions and, to restrict input from each eye to one hemisphere, section of the optic chiasm. Ten controls received either bilateral temporal lesions alone, chiasm section alone or remained unoperated. Only the experimental animals showed impaired transfer. These results suggest that inferior temporal neurons mediate interhemispheric transfer by providing perceptual equivalence for patterns in the left and right visual fields, and, by implication, perhaps also for patterns in different parts of the same field.

Neurons in inferotemporal cortex respond only to visual stimuli and a majority have receptive fields that extend well into both visual half-fields. After bilateral removal of striate cortex, no inferotemporal neurons responded to visual stimuli. After unilateral removal of striate cortex, inferotemporal neurons in both hemispheres responded only to stimuli in the hemifield contralateral to the intact striate cortex. After section of the corpus callosum and anterior commissure, inferotemporal neurons in both hemispheres responded only to stimuli in the hemifield contralateral to the recording site. These results indicate that inferotemporal cortex visual information from striate cortex and that the pathway from striate cortex to the contralateral inferotemporal cortex includes the forebrain commissures. This same striate-temporal pathway is also necessary for normal discrimination learning. We suggest that the converging input onto single inferotemporal neurons from widely separated retinal areas may provide a mechanism for stimulus equivalence over different parts of the visual field, and it may be the absence of such a mechanism that contributes to the visual discrimination deficit that follows inferotemporal lesions.

The inferior temporal (IT) cortex of 6 macaques was injected with horseradish peroxidase. HRP-labeled cells were found throughout IT cortex itself (outside the injection area) but were not found in the polysensory areas that surround IT dorsally, anteriorly and ventrally. Posterior to IT, labeled cells were found in the anterior parts of prestriate cortex. In one animal, the anterior prestriate region was injected with HRP. Labeled cells were then found in the regions of posterior prestriate cortex that receive direct projections from striate cortex. These results suggest that IT cortex receives information from striate cortex after at least two stages of processing in prestriate cortex.

Previous studies have reported that some neurons in the inferior temporal (IT) cortex respond selectively to highly specific complex objects. In the present study, we conducted the first systematic survey of the responses of IT neurons to both simple stimuli, such as edges and bars, and highly complex stimuli, such as models of flowers, snakes, hands, and faces. If a neuron responded to any of these stimuli, we attempted to isolate the critical stimulus features underlying the response. We found that many of the responsive neurons responded well to virtually every stimulus tested. The remaining, stimulus-selective cells were often selective along the dimensions of shape, color, or texture of a stimulus, and this selectivity was maintained throughout a large receptive field. Although most IT neurons do not appear to be "detectors" for complex objects, we did find a separate population of cells that responded selectively to faces. The responses of these cells were dependent on the configuration of specific face features, and their selectivity was maintained over changes in stimulus size and position. A particularly high incidence of such cells was found deep in the superior temporal sulcus. These results indicate that there may be specialized mechanisms for the analysis of faces in IT cortex.

Inferior temporal cortex plays an important role in shape recognition. To study the shape selectivity of single inferior temporal neurons, we recorded their responses to a set of shapes systematically varying in boundary curvature. Many inferior temporal neurons were selective for stimuli of specific boundary curvature and maintained this selectivity over changes in stimulus size or position. The method of describing boundary curvature was that of Fourier descriptors.

Monkeys with inferior temporal cortex lesions and unoperated monkeys were trained to discriminate pairs of objects and then tested for transfer after the original discriminanda were made larger or smaller, rotated, or presented as two-dimensional projections. The two groups of monkeys transferred equally well to the discriminanda altered in size or orientation, but only the unoperated animals transferred to the two-dimensional representation.

Ablation of inferior temporal cortex in the rhesus monkey produces a visual discrimination learning deficit. The severity of this deficit has often been found to be a function of task difficulty. This report concerns a type of visual discrimination problem that, although difficult, is not sensitive to inferior temporal lesions. Monkeys with anterior, posterior, and complete inferior temporal lesions were repeatedly unimpaired or only slightly impaired in learning to discriminate a pattern from the same pattern rotated 90 degrees or 180 degrees; yet they were very severely impaired in learning equally or more difficult discriminations of two different patterns. This demonstration that discrimination of orientation of patterns is relatively spared after inferior temporal lesions helps specify the pattern-recognition processes that require inferior temporal cortex.

Most neurons in the inferior temporal cortex of the rhesus monkeys have visual receptive fields that extend across the vertical meridian well into both the contralateral and ipsilateral visual half-fields. We examined the role of different portions of the forebrain commissures in providing the ipsilateral input with the following results. (1) Combined section of the splenium and anterior commissure eliminated visual activation from the ipsilateral visual half-field. (2) Section of the splenium, with sparing of the anterior commissure, reduced the incidence of ipsilateral activation by about one-half. (3) Section of the anterior commissure, with sparing of the splenium, did not alter the incidence of ipsilateral activation. (4) Section of the non-splenial portions of the corpus callosum had no effect on the laterality of the receptive fields. Thus, both the splenium and the anterior commissure but not the non-splenial callosum can provide information from the ipsilateral visual field to neurons in inferior temporal cortex. These results are interpreted as suggesting that the converging input from the two visual half-fields onto single inferior temporal neurons provided by the forebrain commissures may mediate interhemispheric transfer of visual habits.

Neurons in inferotemporal cortex (area TE) of the monkey had visual receptive fields which were very large (greater than 10 by 10 degrees) and almost always included the fovea. Some extended well into both halves of the visual field, while others were confined to the ipsilateral or contralateral side. These neurons were differentially sensitive to several of the following dimensions of the stimulus: size and shape, color, orientation, and direction of movement.