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.     

The latency of activation of neurones in the lateral hypothalamus and substantia innominata during feeding in the monkey

To investigate whether the responses of neurones in the lateral hypothalamus and substantia innominata associated with the sight of food could control the responses of the hungry monkey to the food, the latency of activation of these neurones by food was measured. It was found that when an electromagnetically operated wide-aperture shutter opened to reveal food or non-food objects, these hypothalamic neurones responded with a latency of 150–200 msec to the food objects, and did not respond to the non-food objects. To measure the latency of the monkey's responses to the food, a visual discrimination task was set in which the monkey could lick a tube to obtain fruit juice if a food-related visual stimulus was shown, but obtained hypertonic saline, which was aversive, if a different visual stimulus was shown. In this situation the typical latencies of the neuronal responses to the food were 150–200 msec, of the lick responses 350–400 msec. and of the EMG activity associated with these lick responses 250–400 msec. Thus the responses of these hypothalamic neurones precede the monkey's responses to the food, and could mediate the feeding and other responses of the animal to the food.It was also shown that a different population of hypothalamic neurones with responses associated with the sight of aversive visual stimuli had response latencies of 150–200 msec.     

The representation of Kanizsa illusory contours in the monkey inferior temporal cortex

Stimulus reduction is an effective way to study visual performance. Cues such as surface characteristics, colour and inner lines can be removed from stimuli, revealing how the change affects recognition and neural processing. An extreme reduction is the removal of the very stimulus, defining it with illusory lines. Perceived boundaries without physical differences between shape and background are called illusory (or subjective) contours. Illusory and real contours activate early stages of the macaque visual pathway in similar ways. However, data relating to the processing of illusory contours in higher visual areas are scarce. We recently reported how illusory contours based on abutting‐line gratings affect neurones in the monkey inferotemporal cortex, an area essential for object and shape vision. We now present data on how inferotemporal cortical neurones of monkeys react to another type of shapes, the Kanizsa figures. A set of line drawings, silhouettes, their illusory contour‐based counterparts, and control shapes have been presented to awake, fixating rhesus monkeys while single‐cell activity was recorded in the anterior part of the inferotemporal cortex. Most of the recorded neurones were responsive and selective to shapes presented as illusory contours. Shape selectivity was proved to be different for line drawings and illusory contours, and also for silhouettes and illusory contours. Neuronal response latencies for Kanizsa figures were significantly longer than those for line drawings and silhouettes. These results reveal differences in processing for Kanizsa figures and shapes having real contours in the monkey inferotemporal cortex.     

Changes in neuronal activity related to the repetition and relative familiarity of visual stimuli in rhinal and adjacent cortex of the anaesthetised rat

Employing the same techniques as have been used with conscious rats, this study describes neuronal responses signalling information concerning the prior occurrence of visual stimuli in unconscious rats. Recordings of the activity of 387 neurones were made while anaesthetised rats were shown objects. Changes in neuronal responses related to stimulus repetition and the relative familiarity of visual stimuli were sought. The areas sampled were lateral occipital cortex, area TE of temporal cortex, perirhinal cortex and the hippocampal formation. The response to the first presentations of unfamiliar objects was significantly different from that to their second presentations for 30 (35%) of 86 visually responsive neurones; for 23 of the neurones was smaller when the stimulus was repeated, whereas for 7 it was larger. For all of these neurones the response change was maintained across intervening trials on which other stimuli were shown. For 4 (25%) of 16 neurones so tested, the response decrement persisted across at least 10 intervening trials. The activity of 63 neurones was recorded while rats were shown highly familiar as well as unfamiliar objects. The response to unfamiliar objects was significantly different from that to highly familiar objects for 3 (23%) of 13 visually responsive neurones. The types of neuronal response and their incidence expressed as a proportion of the number of visually responsive neurones were similar to those found in unanaesthetised rats (though the proportion of visually responsive neurones encountered in the anaesthetised rat was lower). The results indicate that information concerning the prior occurrence of stimuli is processed even under anaesthesia.     

Modulation during learning of the responses of neurons in the lateral hypothalamus to the sight of food

Recordings were made from single neurons in the lateral hypothalamus and substantia innominata of the rhesus and squirrel monkey during feeding. A population of these neurons which altered their firing rates while the monkeys looked at food but not at nonfood objects was investigated. Because the responses of these neurons must have been affected by the previous experience of the animals, the activity of the neurons was measured during tasks in which the monkeys learned whether or not objects which they saw were associated with food. During visual discrimination tests these neurons came to respond when the monkey saw one stimulus associated with food (e.g., a black syringe from which the animal was fed glucose), but not when the monkey saw a different stimulus which was not associated with food (e.g., a white syringe from which the animal was offered saline). During extinction tests these units ceased to respond when the monkey saw a visual stimulus such as a peanut if the peanut was repeatedly not given to the monkey to eat. The learning or extinction behavior approximately paralleled the response of the neurons.The findings that the neurons in the lateral hypothalamus and substantia innominata respond when a monkey is shown food only if he is hungry, and as shown here, if as a result of learning the visual stimulus signifies food, provide information on a part of the brain which may be involved in feeding. The findings are consistent with other data which suggest that the responses of these neurons are involved in the autonomic and/or behavioral reactions of the animal to the sight of food.     

Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory

Amnesia has been reported to result from combined damage to the amygdala, hippocampus and inferomedial temporal cortex in man and monkey. Evidence is presented that neuronal activity in the monkey inferomedial temporal cortex reflects memory for the previous occurrence of visual stimuli: 26 (15%) of 173 single units responded more strongly to first than to subsequent presentation of unfamiliar stimuli. No such responses were found for neurones recorded in the hippocampus and subicular cortex. The findings suggest that the inferomedial temporal cortex plays a central role in processes necessary for recognition memory.     

Crossed unilateral lesions of temporal lobe structures and cholinergic cell bodies impair visual conditional and object discrimination learning in monkeys

Monkeys with excitotoxic lesions of the CA1/subiculum region in the right hemisphere and with immunotoxic lesions of the cholinergic cells of the diagonal band in the left hemisphere were impaired on a visual conditional task. In this task, correct choice of one of two objects depends on which of two background fields both objects are presented against, irrespective of the spatial positions of the objects. They were not impaired on simple object or shape discrimination tasks. The pattern of impairments is the same as that seen after bilateral excitotoxic lesions of CA1/subiculum, implying that the diagonal band lesion disables the ipsilateral CA1/subiculum. It also argues that CA1/subiculum, sustained by its cholinergic input, is necessary for some forms of nonspatial conditional learning. Addition of an inferotemporal (IT) cortical ablation to the left hemisphere did not affect simple visual discrimination learning, although all the monkeys then failed to learn a new visual conditional task. This demonstrates that intact IT cortex in only one hemisphere is sufficient to sustain simple visual discrimination learning but implies that the cholinergic input and the inferotemporal cortical input to the hippocampus both contribute to visual conditional learning. The subsequent addition of an immunotoxic lesion of the basal nucleus of Meynert in the right hemisphere resulted in an additional impairment on a difficult shape discrimination. This argues that it is the cholinergic projection to the inferotemporal cortex, rather than to the rest of the cortex, which contributes to visual discrimination learning and memory.     

Unit activity in the hippocampus and the parahippocampal temporobasal association cortex related to memory and complex behaviour in the awake monkey

Monkeys (Macaca fascicularis) were trained on a delayed match-to-sample (DMS) task using delays of upto 20 s. Unit activity was recorded from the hippocampus and the temporo-basal association cortex in the lateral parahippocampal region (partly corresponding to TF and TH) during the DMS task, as well as during a visual object discrimination task and some behavioural situations involving the experimenter. Units were encountered that gave visual responses which were sometimes context-dependent. Changes in discharge rate during the delay period of the DMS task were very rare and when present, very weak. On the other hand, many neurones, including some of those which were unresponsive during the DMS task fired vigorously (or were inhibited) during situations which involved attention, expectation or food consumption. For example, the neurones' firing rate was altered when the cage door was opened or closed, the experimenter entered or left the room or showed the monkey a piece of food before giving it to him. A variety of such responses in complex behavioural situations were seen, sometimes even in neurones which did not respond in the DMS task. Activity changes in neurons of the temporo-basal cortex thus appear to be related to the internal state associated with a stimulus and even some of the responses obtained in the DMS task can be interpreted as being related to changes in the behavioural state rather than to the mnemonic elements of the task.     

Neurophysiological analysis of brain-stimulation reward in the monkey

Neuronal activity related to brain-stimulation reward and to feeding was analyzed in rhesus monkeys and squirrel monkeys as follows. First, self-stimulation of the lateral hypothalamus, orbitofrontal cortex, amygdala and nucleus accumbens was found. Second, a population of single neurones in the lateral hypothalamus was found to be trans-synaptically activated from one or several self-stimulation sites. It was also found that populations of neurones in the orbitofrontal cortex and amygdala were activated from at least some of the self-stimulation sites. Thus, in the monkey, there is evidence for an interconnected set of self-stimulation sites, stimulation in any one of which may activate neurones in the other regions. These sites include the lateral hypothalamus, amygdala, and orbitofrontal cortex. Third, in one sample of 764 neurones in the lateral hypothalamis and substantia innominata which were activated from brain-stimulation reward sites, 13.6% were also activated during feeding, by the sight and/or taste of food. The responses of the neurones with activity associated with taste occurred only while some substances (e.g. sweet substances such as glucose) were in the mouth, depended on the concentration of the substances being tasted, and were independent of mouth movements made by the monkeys. Fourth, the responses of these neutrones occurre to food when the monkeys were hungry, but not when they were satiated. Fifth, self-stimulation occurred in the region of these neurones in the lateral hypothalamus and substantia innominata, and was attenuated by satiety. These results suggest that self-stimulation of some brain sites occurs because of activation of neurones in the lateral hypothalamus and substantia innominata activated by the sight and/or taste of food in the hungry animal, and that these neurones are involved in responses to food reward.     

Modification of the responses of hippocampal neurons in the monkey during the learning of a conditional spatial response task

In order to analyze the function of the hippocampus in learning, the activity of single neurons was recorded while monkeys learned a task of the type known to be impaired by damage to the hippocampus. In the conditional response task, the monkey had to learn to make one response when one stimulus was shown, and a different response when a different stimulus was shown. It had previously been shown that there are neurons in the hippocampal formation that respond in this task, to, for example, a combination of a particular visual stimulus that had been associated in previous learning with a particular behavioral response. In the present study, it was found that during such conditional response learning, the activity of 22% of the neurons in the hippocampus and parahippocampal gyrus with activity specifically related to the task altered their responses so that their activity, which was initially equal to the two new stimuli, became progressively differential to the two stimuli when the monkey learned to make different responses to the two stimuli. These changes occurred for different neurons just before, at, or just after the time when the monkey learned the correct response to make to the stimuli. In addition to these neurons, which had differential responses that were sustained for as long as the recordings continued, another population of neurons (45% of those with activity specifically related to the task) developed differential activity to the two new stimuli, yet showed such differential responses transiently for only a small number of trials at about the time when the monkey learned. These findings are consistent with the hypothesis that some synapses on hippocampal neurons modify during this type of learning so that some neurons come to respond to particular stimulus-response associations that are being learned. Further, the finding that many hippocampal neurons started to reflect the new learning, but then stopped responding differentially (the transient neurons), is consistent with the hypothesis that the hippocampal neurons with large sustained changes in their activity inhibited the transient neurons, which then underwent reverse learning, thus providing a competitive mechanism by which not all neurons are allocated to any one learned association or event.     

Neurotoxic lesions of ventrolateral prefrontal cortex impair object-in-place scene memory

Disconnection of the frontal lobe from the inferotemporal cortex produces deficits in a number of cognitive tasks that require the application of memory-dependent rules to visual stimuli. The specific regions of frontal cortex that interact with the temporal lobe in performance of these tasks remain undefined. One capacity that is impaired by frontal-temporal disconnection is rapid learning of new object-in-place scene problems, in which visual discriminations between two small typographic characters are learned in the context of different visually complex scenes. In the present study, we examined whether neurotoxic lesions of ventrolateral prefrontal cortex in one hemisphere, combined with ablation of inferior temporal cortex in the contralateral hemisphere, would impair learning of new object-in-place scene problems. Male macaque monkeys learned 10 or 20 new object-in-place problems in each daily test session. Unilateral neurotoxic lesions of ventrolateral prefrontal cortex produced by multiple injections of a mixture of ibotenate and N-methyl-D-aspartate did not affect performance. However, when disconnection from inferotemporal cortex was completed by ablating this region contralateral to the neurotoxic prefrontal lesion, new learning was substantially impaired. Sham disconnection (injecting saline instead of neurotoxin contralateral to the inferotemporal lesion) did not affect performance. These findings support two conclusions: first, that the ventrolateral prefrontal cortex is a critical area within the frontal lobe for scene memory; and second, the effects of ablations of prefrontal cortex can be confidently attributed to the loss of cell bodies within the prefrontal cortex rather than to interruption of fibres of passage through the lesioned area.     

Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food

Recordings were made from single neurons in the monkey lateral hypothalamus and substantia innominata which had previously been shown to respond with an increase or decrease of their firing rates when the hungry monkey tasted food, and/or when he looked at food. It was found that the responsiveness of these neurons to food decreased over the course of a meal of glucose as satiety increased. When satiety, measured by whether the monkey rejected the glucose, was complete, there was no response of the neurons to the taste and/or to the sight of glucose. The spontaneous firing rates of these cells were not affected by the transitions from hunger to satiety. This modulation of responsiveness to food of hypothalamic cells was specific to them in that it was not seen in cells in the globus pallidus which responded in relation to swallowing and mouth movements, or in cells in the visual inferotemporal cortex which responded when the monkey looked at the glucose-containing syringe. On the basis of this and other evidence it is suggested that the hypothalamic cells described here could be involved in the autonomic, the endocrine, and/or the feeding responses which occur when an animal sees or tastes food.     

Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys

Cynomolgus monkeys (Macaca fascicularis) were trained in a task that assessed their ability to associate visual stimuli with food reward. Acquisition of stimulus-reward associations was measured under 2 conditions, a 2-stimuli acquisition condition and a 1-stimulus acquisition condition. On each trial in the 2-stimuli condition, the positive (correct) and negative (incorrect) stimuli were presented side by side and the animal chose one by touching it; if the choice was correct, a food reward was dispensed. On each trial in the 1-stimulus condition, either the positive or the negative stimulus was presented alone; if the stimulus was the positive, it was followed by reward delivery, regardless of the animal's response to it, and if it was the negative, it was not followed by reward delivery. Thus, reward delivery was contingent upon the animal's response to the stimuli in the 2-stimuli condition but not in the 1-stimulus condition. The effect of acquisition trials under these 2 conditions was measured, in both conditions, by the animal's subsequent choice when presented with the 2 stimuli side by side. Following preoperative training in this task, the animals were first subjected to unilateral ablation of the inferotemporal cortex. This operation had little effect on the animals' learning ability. Then, the amygdala was ablated in the hemisphere contralateral to that in which the unilateral inferotemporal ablation had been carried out. This combination of crossed unilateral lesions of the amygdala and of the inferotemporal cortex, which disconnects the amygdala from the output of visual association cortex, produced a profound impairment in stimulus-reward-associative learning.(ABSTRACT TRUNCATED AT 250 WORDS)     

Activity of neurons in monkey posterior temporal cortex during multidimensional visual discrimination tasks

Unit activity was recorded from the posterior temporal cortex (PTE) of awake, behaving rhesus monkeys while they performed a series of visual discrimination tasks involving colored checkerboard patterns. The activity of 130 (91%) of 143 PTE units was altered by the presentation of a visual discriminandum; 112 of these cells (86%) exhibited a significant increase in firing after presentation of the stimulus while the remainder gave an inhibitory response. Over half (64%) the PTE units exhibited differential activity between discriminanda, i.e. they were selective for color and/or form. Six of 10 neurons, recorded when the monkey was required to shift attention from one stimulus feature to another, exhibited a difference in poststimulus neural activity even though the discriminandum remained the same. Three neurons were recorded from when the stimuli were altered by changing the check size although the relevant (i.e. rewarded) dimension (color) was left the same; two showed an invariant response to the altered stimuli and one gave the same response to one of the altered stimuli but a different response to the other. These data support the role of posterior temporal cortex in visual discrimination learning and visual attention.     

Visual agnosia and Klüver-Bucy syndrome in marmosets (Callithrix jacchus) following ablation of inferotemporal cortex, with additional mnemonic effects of immunotoxic lesions of cholinergic projections to medial temporal areas

Inferotemporal ablations in the New World monkey, the common marmoset (Callithrix jacchus), produced a persistent impairment on visual discrimination learning and a florid, but transient, Klüver-Bucy syndrome. Monkeys with these ablations were impaired on acquisition of object discriminations to a high criterion and on concurrent discrimination learning, to a single high criterion across all trials. Neither the control monkeys nor the monkeys with inferotemporal ablations found acquisition more difficult when the component discriminations of a set were presented concurrently compared to consecutively, although the monkeys with inferotemporal ablations found acquisition under both these conditions somewhat more difficult than did control monkeys. This suggests that the severe impairment caused by inferotemporal ablations on concurrent learning measured across all trials is due to the need for sustained performance across a concurrent set rather than to the extra mnemonic demands of concurrent presentation. When immunotoxic lesions of the cholinergic projection to the hippocampal formation were added to the inferotemporal ablations, a further impairment on retention, and a differential impairment on concurrent, compared to consecutive, learning was observed. Previous studies have shown that lesions of the cholinergic projection to the hippocampus alone, or excitotoxic hippocampal lesions, do not affect simple visual discrimination learning. It is suggested that large inferotemporal ablations in monkeys produce a visual agnosia which causes severe 'psychic blindness' in the first instance, and a persistent impairment on visual discrimination learning. The hippocampus makes a contribution, which may be mnemonic, to discrimination performance after inferotemporal ablations.     

Visual agnosia and Klüver–Bucy syndrome in marmosets (Callithrix jacchus) following ablation of inferotemporal cortex, with additional mnemonic effects of immunotoxic lesions of cholinergic projections to medial temporal areas

Inferotemporal ablations in the New World monkey, the common marmoset (Callithrix jacchus), produced a persistent impairment on visual discrimination learning and a florid, but transient, Klüver–Bucy syndrome. Monkeys with these ablations were impaired on acquisition of object discriminations to a high criterion and on concurrent discrimination learning, to a single high criterion across all trials. Neither the control monkeys nor the monkeys with inferotemporal ablations found acquisition more difficult when the component discriminations of a set were presented concurrently compared to consecutively, although the monkeys with inferotemporal ablations found acquisition under both these conditions somewhat more difficult than did control monkeys. This suggests that the severe impairment caused by inferotemporal ablations on concurrent learning measured across all trials is due to the need for sustained performance across a concurrent set rather than to the extra mnemonic demands of concurrent presentation. When immunotoxic lesions of the cholinergic projection to the hippocampal formation were added to the inferotemporal ablations, a further impairment on retention, and a differential impairment on concurrent, compared to consecutive, learning was observed. Previous studies have shown that lesions of the cholinergic projection to the hippocampus alone, or excitotoxic hippocampal lesions, do not affect simple visual discrimination learning. It is suggested that large inferotemporal ablations in monkeys produce a visual agnosia which causes severe ‘psychic blindness’ in the first instance, and a persistent impairment on visual discrimination learning. The hippocampus makes a contribution, which may be mnemonic, to discrimination performance after inferotemporal ablations.     

Responses of macaque perirhinal neurons during and after visual stimulus association learning.

Recent lesion studies have implicated the perirhinal cortex in learning that two objects are associated, i.e., visual association learning. In this experiment we tested whether neuronal responses to associated stimuli in perirhinal cortex are altered over the course of learning. Neurons were recorded from monkeys during performance of a visual discrimination task in which a predictor stimulus was followed, after a delay, by a GO or NO-GO choice stimulus. Association learning had two major influences on neuronal responses. First, responses to frequently paired predictor-choice stimuli were more similar to one another than was the case with infrequently paired stimuli. Second, the magnitude of activity during the delay was correlated with the magnitude of responses to both the predictor and choice stimuli. Both of these learning effects were found only for stimulus pairs that had been associated on at least 2 d of training. Early in training, the delay activity was correlated only with the response to the predictor stimuli. Thus, with long-term training, perirhinal neurons tend to link the representations of temporally associated stimuli.     

Development of monotonic neuronal tuning in the monkey inferotemporal cortex through long-term learning of fine shape discrimination

Visual expertise in discriminating fine differences among a group of similar objects can be obtained through extensive long-term training. Here we investigated the neural bases of this superior capability. The inferotemporal cortex, located at the final stage along the ventral visual pathway, was a candidate site in monkeys because cells there respond to various complex features of objects. To identify the changes that underlie the development of visual expertise in fine discrimination, we created a set of parametrically designed object stimuli and compared the stimulus selectivity of inferotemporal cells between two different training histories. One group of recordings was conducted after the monkeys had been extensively trained for fine discrimination (fine-discrimination period) and the other after the monkeys had been exposed only for coarse discrimination (coarse-discrimination period). We found that the tuning of responses recorded in the fine-discrimination period was more monotonic in the stimulus parameter space. The stimuli located at the extreme in the parameter space evoked the maximum responses in a larger proportion of cells and the direction of response decrease in the parameter space was more consistent. Moreover, the stimulus arrangement reconstructed from the responses recorded during the fine-discrimination period was more similar to the original stimulus arrangement. These results suggest that visual expertise could be based on the development, in the inferotemporal cortex, of neuronal selectivity monotonically tuned over the parameter space of the object images.     

Hippocampus and medial temporal cortex: neuronal activity related to behavioural responses during the performance of memory tasks by primates

Neuronal activity was recorded in the hippocampal formation, the parahippocampal gyrus and medial inferotemporal cortex of monkeys performing memory tasks. In a modified delayed matching to sample task in which 2 sequentially presented stimuli were compared on each trial, a match condition required a right panel press, whereas a non-match condition required a left panel press. The activity of 336/736 (45.7%) neurons was related to the behavioural responses (left or right panel presses) in this task. The incidence of response-related activity was 57.4% in cortical areas adjacent to the rhinal sulcus plus medial inferotemporal cortex, and 40.2% for the hippocampal formation. For 58.9% of these response-related neurons, the activity change associated with the behavioural response was greater than that during presentation of the sensory stimuli, though neurons commonly responded (33.2% of all recorded neurons) to both sensory and motor events. The activity of 198 neurons (26.9%) differed between go-left and go-right trials; such neurons were found in all areas but were nearly twice as common in the posterior as in the anterior hippocampal formation. The importance of visual stimuli for the response-related neuronal activity was examined during the performance of a delayed alternation task without visual cues indicating direction of response. The response-related activity of 8 neurons recorded during the delayed alternation and the delayed matching tasks was similar in both tasks, indicating that memory for the behavioural responses influences the activity of the response-related neurons. In order to test the effects of stimulus familiarity and non-spatial responses on medial temporal neurons, recognition memory and visual discrimination tasks requiring lick responses were performed. The activity of 2/375 (0.5%) neurons was related to the lick responses; 3/68 neurons in the inferomedial temporal cortex responded on the basis of stimulus novelty and none reflected their reinforcement value. It is concluded that the hippocampal formation, the parahippocampal gyrus and medial inferotemporal cortex all have a role in the utilisation of sensory, mnemonic and motor information underlying the selection of spatially-directed behavioural responses.     

Occipital and inferotemporal responses to visual signals in the monkey

This study analyzes cellular and field-potential responses in striate and inferotemporal cortex to visual stimuli in monkeys performing a memory task (delayed matching-to-sample). Each trial was initiated by a brief alerting diffuse flash preceding presentation of the memorandum (sample); the latter was a lighted circle (red or green, 1.5 s) to be retained by the animal during a subsequent delay for correct behavioral response (color match). The alerting flash evoked distinct excitatory cell responses and field potentials in the occipital cortex; those two orders of phenomena were broadly related to each other in temporal terms. By contrast, most cells in the inferotemporal region were inhibited by the flash, although the local evoked field potential had a configuration similar to that of the occipital potential. In each region, the sample stimuli elicited excitatory unit responses which summed to a unimodal distribution with an initial component roughly corresponding in time course to the local field potential. Although the shortest response latencies were found in occipital cortex, considerable temporal overlap of the sample-related activities in the two cortices was observed. The finding that most inferotemporal cells, unlike occipital cells, treated only the sample with excitatory response indicates that the inferotemporal cortex is selectively attuned to visual detail. However, the largely simultaneous activation of both cortical regions following the onset of the sample suggests that discriminative visual information is processed by hierarchic interactions of the two cortices through their reciprocal connections.