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E T Rolls

Publications and source records attributed to E T Rolls.

At least 109 records · Page 6Linked to original sources

Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas.

The ways in which information about faces is represented and stored in the temporal lobe visual areas of primates, as shown by recordings from single neurons in macaques, are considered. Some neurons that respond primarily to faces are found in the cortex in the anterior part of the superior temporal sulcus (in which neurons are especially likely to be tuned to facial expression and to face movement involved in gesture), and in the TE areas more ventrally forming the inferior temporal gyrus (in which neurons are more likely to have responses related to the identity of faces). Quantitative studies of the responses of the neurons that respond differently to the faces of different individuals show that information about the identity of the individual is represented by the responses of a population of neurons, that is, ensemble encoding rather than 'grandmother cell' encoding is used. It is argued that this type of tuning is a delicate compromise between very fine tuning, which has the advantage of low interference in neuronal network operations but the disadvantage of losing the useful properties (such as generalization, completion and graceful degradation) of storage in neuronal networks, and broad tuning, which has the advantage of allowing these properties of neuronal networks to be realized but the disadvantage of leading to interference between the different memories stored in an associative network. There is evidence that the responses of some of these neurons are altered by experience so that new stimuli become incorporated in the network. It is shown that the representation that is built in temporal cortical areas shows considerable invariance for size, contrast, spatial frequency and translation. Thus the representation is in a form which is particularly useful for storage and as an output from the visual system. It is also shown that one of the representations that is built is object based, which is suitable for recognition and as an input to associative memory, and that another is viewer centred, which is appropriate for conveying information about gesture. Ways are considered in which such cortical representations might be built by competitive self-organization aided by back projections in the multi-stage cortical processing hierarchy which has convergence from stage to stage.

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Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network.

The CA3 network in the hippocampus may operate as an autoassociator, in which declarative memories, known to be dependent on hippocampal processing, could be stored, and subsequently retrieved, using modifiable synaptic efficacies in the CA3 recurrent collateral system. On the basis of this hypothesis, the authors explore the computational relevance of the extrinsic afferents to the CA3 network. A quantitative statistical analysis of the information that may be relayed by such afferent connections reveals the need for two distinct systems of input synapses. The synapses of the first system need to be strong (but not associatively modifiable) in order to force, during learning, the CA3 cells into a pattern of activity relatively independent of any inputs being received from the recurrent collaterals, and which thus reflects sizable amounts of new information. It is proposed that the mossy fiber system performs this function. A second system, with a large number of associatively modifiable synapses on each receiving cell, is needed in order to relay a signal specific enough to initiate the retrieval process. This may be identified, we propose, with the perforant path input to CA3.

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Oscillatory activity is not evident in the primate temporal visual cortex with static stimuli.

It has been suggested in studies in the visual system of anaesthetized cats that oscillatory activity with a frequency of 40-60 Hz occurs during the presentation of moving visual stimuli and reflects a synchronization process between neurons that could implement the binding together of related neurons into different sets. We found no evidence for such oscillations in the inferior temporal visual cortex and related areas of awake macaques fixating effective static visual stimuli, which for the neurons analysed were faces. We put forward the possibility that temporal synchronization between neurons to implement binding may not be generally used in the visual system as a solution to the binding problem, at least when static objects are being processed and recognised in higher parts of the visual system.

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Potentiation of neuronal responses to natural visual input paired with postsynaptic activation in the hippocampus of the awake monkey.

Extracellular recordings were made in the hippocampal formation while the monkey performed a simple visual discrimination task in which the stimuli consisted of coloured patterns presented serially. By using this natural visual input to single hippocampal neurones, and experimentally pairing one of the stimuli with postsynaptic excitation induced by iontophoretically applied L-glutamate, we demonstrate that selective synaptic potentiation can result. Seven of 29 neurones tested showed potentiation. The potentiation was selective in that enhanced responses only occurred to the previously paired stimulus, and not to other visual stimuli. The potentiation was observed in CA3 neurones and lasted approximately 15 min. In each case the latency of the potentiated response occurred at 160 ms following the onset time of the stimulus.

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Responses of neurons in the primate taste cortex to glutamate.

In order to investigate the neural encoding of glutamate in the primate, recordings were made from 190 taste responsive neurons in the primary taste cortex and adjoining orbitofrontal cortex taste area in macaques. Single neurons were found that were tuned to respond best to glutamate (umami taste), just as other cells were found with best responses to glucose (sweet), sodium chloride (salty), HCl (sour), and quinine HCl (bitter). Across the population of neurons, the responsiveness to glutamate was poorly correlated with the responsiveness to NaCl, so that the representation of glutamate was clearly different from that of NaCl. Further, the representation of glutamate was shown to be approximately as different from each of the other four tastants as they are from each other, as shown by multidimensional scaling and cluster analysis. Moreover, it was found that glutamate is approximately as well represented in terms of mean evoked neural activity and the number of cells with best responses to it as the other four stimuli, glucose, NaCl, HCl and quinine. It is concluded that in primate taste cortical areas, glutamate, which produces umami taste in humans, is approximately as well represented as are the tastes produced by: glucose (sweet), NaCl (salty), HCl (sour) and quinine HCl (sour).

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Delay, discriminatory, and modality specific neurons in striatum and pallidum during short-term memory tasks.

The function of the striatum and its integrative capacities is addressed. The activity of single neurons in behaving Macaca mulatta is studied. Two new classes of neurons were found. In the striatum, but not in the pallidum, these neurons were visual modality specific. These neurons may represent a conjunction of sensory, mnemonic and motor information, and may be concerned with decisions about the emission or withholding of movements. The frontal dysfunction hypothesis of cognitive deficits in Parkinson's disease is considered.

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Neuronal responses related to reinforcement in the primate basal forebrain.

In the present study neurones recorded in the substantia innominata, the diagonal band of Broca and a periventricular region of the basal forebrain responded differentially to stimuli signalling the availability of fruit juice or saline obtained by making lick responses in two different visual discrimination tasks. The activity of certain neurones reflected the rewarding nature of stimuli used to signal the availability of juice in the tasks, responding to the sight and delivery of both foods and syringes used to deliver juice in tests in which behavioural responses were irrelevant. The activity of other neurones reflected aversion, responding to task stimuli signalling availability of saline and to syringes used to deliver saline to the mouth. In another task an auditory cue that signalled the availability of juice elicited neuronal responses. These neurones also responded to a tone cue used to signal the onset of the trial, and during certain mouth and arm movements which the monkey used to obtain reinforcement. The responses of these differential neurones were similar in most respects in all 3 regions of the basal forebrain. Thus these neurones respond to a range of visual and auditory stimuli that monkeys have learned can be used to obtain reinforcement, but not on the basis of sensory properties such as shape or colour of the stimuli. We conclude that the reinforcement-related nature of the neuronal signal from the basal forebrain could be used to facilitate processing in cortical regions, optimising the functioning of sensory, motor and association cortices, thus increasing the probability of responding appropriately to learned environmental contingencies. We suggest that the properties of these neurones are due to afferent inputs from ventromedial regions of the prefrontal and temporal cortices and amygdala.

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Neuronal responses related to the novelty and familarity of visual stimuli in the substantia innominata, diagonal band of Broca and periventricular region of the primate basal forebrain.

This study examined correlates of memory processes in neuronal activity recorded from the substantia innominata, the diagonal band of Broca and the periventricular region or the basal forebrain of monkeys performing recognition and/or visual discrimination tasks. Two types of neurons were found that responded differentially to stimuli on the basis of their novelty or their familiarity. Neurons (5/572) in the periventricular region rostral to the thalamus and caudal to the anterior commissure responded to familiar stimuli with increases in firing rate. Neurons in the substantia innominata (16/1058) and in the diagonal band (14/489) responded maximally to novel stimuli, with smaller responses to reappeared presentations of these stimuli. The properties of these two types of neurons were similar in three respects: (1) the magnitude of the differential response to novel and familiar presentations of stimuli were largest for stimuli presented on successive trials, and were attenuated for stimuli that had not been seen for some intervening trials; (2) both types of neurons responded to highly familiar stimuli as if they were novel if they had not been recently seen; (3) both types responded to two- and three-dimensional stimuli; and were recorded in rhesus monkeys trained on the recognition tasks and in untrained cynomolgus monkeys. An injection of HRP into the periventricular region of one monkey resulted in retrograde labeling of ventromedial regions of the prefrontal, cingulate and temporal cortices, of the amygdala, medial thalamus, supramammillary region of the midbrain. These data indicate that information about the novelty, familiarity or recency of presentation of visual stimuli is reflected in the responses of some basal forebrain neurons. Neurons in the substantia innominata and diagonal band of Broca could not be distinguished using the battery of applied tests, suggesting functional mechanisms common to both regions. The results of the anatomical experiment suggest that ventromedial limbic cortical and subcortical regions projecting to or through the periventricular region may be important for the transmission of information about visual stimuli and for memory function.

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Gustatory responses of single neurons in the insula of the macaque monkey.

1. In recordings made from 2,925 single neurons, a region of primary taste cortex was localized to the rostral and dorsal part of the insula of the cynomolgus macaque monkey, Macaca fascicularis. The area is part of the dysgranular field of the insula and is bordered laterally by the frontal opercular taste cortex. 2. The responses of 65 single neurons with gustatory responses were analyzed in awake macaques with the use of the taste stimuli glucose, NaCl, HCl, quinine HCl (QHCl), water, and black currant juice. 3. Intensity-response functions showed that the lowest concentration in the dynamic part of the range conformed well to human thresholds for the basic taste stimuli. 4. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a neuron that responds specifically to only one of the four basic taste stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 65 cells in the taste insula was 0.56. This tuning is sharper than that of neurons in the nucleus of the solitary tract of the monkey, and similar to that of neurons in the primary frontal opercular taste cortex. 5. A cluster analysis showed that at least six different groups of neurons were present. For each of the taste stimuli, glucose, NaCl, HCl, QHCl, water, and black currant juice, there was one group of neurons that responded much more to that tastant than to the other tastants. Other subgroups of these neurons responded to two or more of these tastants, such as glucose and black currant juice, or NaCl and QHCl. 6. On the basis of this and other evidence, it is concluded that the primary insular taste cortex, in common with the primary frontal opercular taste cortex, represents a stage of information processing in the taste system of the primate at which the tuning of neurons has become sharper than that of neurons in the nucleus of the solitary tract, and is moving toward the fineness achieved in the secondary taste cortex in the caudolateral orbitofrontal taste cortex, where motivation-dependence first becomes manifest in the taste system.

Action Potentials↗

Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey.

1. In recordings made from 3,120 single neurons, a secondary cortical taste area was found in the caudolateral part of the orbitofrontal cortex of the cynomolgus macaque monkey, Macaca fascicularis. The area is part of the dysgranular field of the orbitofrontal cortex and is situated anterior to the primary cortical taste areas in the frontal opercular and adjoining insular cortices. 2. The responses of 49 single neurons with gustatory responses in the caudolateral orbitofrontal taste cortex were analyzed using the taste stimuli glucose, NaCl, HCl, quinine HCl, water, and blackcurrant juice. 3. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a neuron that responds specifically to only one of the four basic taste stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 49 cells in the caudolateral orbitofrontal cortex was 0.39. This tuning is much sharper than that of neurons in the nucleus of the solitary tract of the monkey, and sharper than that of neurons in the primary frontal opercular and insular taste cortices. 4. A cluster analysis showed that at least seven different groups of neurons were present. For each of the taste stimuli glucose, blackcurrant juice, NaCl, and water, there was one group of neurons that responded much more to that tastant than to the other tastants. The other groups of neurons responded to two or more of these tastants, such as glucose and blackcurrant juice. In this particular region neurons were not found with large responses to HCl or quinine HCl, although such neurons could be present in other parts of the orbitofrontal cortex. 5. On the basis of this and other evidence it is concluded that in the caudolateral orbitofrontal cortex there is a secondary cortical taste area in which the tuning of neurons has become finer than in early areas of taste processing, in which foods, water, and NaCl are strongly represented and where motivation dependence first becomes manifest in the taste system.

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Learning and memory is reflected in the responses of reinforcement-related neurons in the primate basal forebrain.

Certain basal forebrain neurons encode the learned reinforcement value of objects: they respond differentially to visual stimuli that signal availability of fruit juice (positively reinforcing) or saline (negatively reinforcing) obtained by lick responses in visual discrimination tasks. In this report we describe the rapid, learning-related changes in the responses of these neurons during the acquisition and reversal of the reinforcement contingency of a visual discrimination reversal task. The same neurons also responded differentially to novel and familiar stimuli in 2 recognition memory tasks, in which monkeys applied the learned rule that lick responses to novel stimuli elicited saline and responses to familiar stimuli elicited juice. These differential responses to novel and familiar stimuli thus reflected the reinforcement value of the stimuli. A single presentation of a novel or a familiar stimulus was sufficient to elicit a differential response which was maintained even when the stimulus had not been seen recently. The maintenance of the differential response indicates that these neurons are influenced by a durable memory for the stimuli, estimated to be 30 trials on average. These differential neurons were recorded in the substantia innominata, the diagonal band of Broca, and a periventricular region of the basal forebrain. The responses of the reinforcement-related neurons in these 3 regions were similar in most respects. These results support the conclusion that basal forebrain neurons respond to sensory stimuli that, through learning of different contingencies, signal the availability of reinforcement. We suggest that the properties of learning and memory reflected in these neuronal responses are due to afferent pathways from ventromedial regions of the prefrontal and temporal cortices and the amygdala, and that the responses of these neurons provide an enabling mechanism that facilitates the operation of diverse cortical regions in which specific sensory, motor, or mnemonic functions take place.

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

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

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

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

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Object-centered encoding by face-selective neurons in the cortex in the superior temporal sulcus of the monkey.

Neurophysiological studies have shown that some neurons in the cortex in the superior temporal sulcus and in the inferior temporal cortex respond to faces. To determine if some face responsive neurons encode stimuli in an object-centered coordinate system rather than a viewer-centered coordinate system, a large number of neurons were tested for sensitivity to head movement in 3 macaque monkeys. Ten neurons responded only when a head undergoing rotatory movements was shown. All of these responded to a particular movement independently of the orientation of the moving head in relation to the viewer, maintaining specificity even when the moving head was inverted or shown from the back, thereby reversing viewer-centered movement vectors. This was taken as evidence that the movement was encoded in object-centered coordinates. In tests of whether there are neurons in this area which respond differently to the faces of different individuals relatively independently of viewing angle, it was found that a further 18 neurons responded more to one static face than another across different views. However, for 16 of these 18 cells there was still some modulation of the neuronal response with viewing angle. These 16 neurons thus did not respond perfectly in relation to the object shown independently of viewing angle, and may represent an intermediate stage between a viewer-centered and an object-centered representation. In the same area as these neurons, other cells were found which responded on the basis of viewer-centered coordinates. These neurophysiological findings provide evidence that some neurons in the inferior temporal visual cortex respond to faces (or heads) on the basis of object-centered coordinates, and that others have responses which are intermediate between object-centered and viewer-centered representations. The results are consistent with the hypothesis that object-centered representations are built in the inferior temporal visual cortex.

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