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Biomedical subjects

E T Rolls

Publications and source records attributed to E T Rolls.

At least 19 recordsLinked to original sources

Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage.

Impairments in the identification of facial and vocal emotional expression were demonstrated in a group of patients with ventral frontal lobe damage who had socially inappropriate behaviour. The expression identification impairments could occur independently of perceptual impairments in facial recognition, voice discrimination, or environmental sound recognition. The face and voice expression problems did not necessarily occur together in the same patients, providing an indication of separate processing. Poor performance on both expression tests was correlated with the degree of alteration of emotional experience reported by the patients. There was also a strong positive correlation between the degree of altered emotional experience and the severity of the behavioural problems (e.g. disinhibition) found in these patients. A comparison group of patients with brain damage outside the ventral frontal lobe region, without these behavioural problems, was unimpaired on the face expression identification test, was significantly less impaired at vocal expression identification and reported little subjective emotional change. The expression identification deficits in ventral frontal patients may contribute to the abnormal behaviour seen after frontal lesions, and have implications for rehabilitation.

Facial Expression

Receiving grooming as a reinforcer for the monkey.

The present study was intended to evaluate whether receiving grooming, given to a monkey by an experimenter, can be used as a positive reinforcer in operant conditioning. When the monkey touched the surface of the correct pattern in a visual discrimination task after a tone cue, the experimenter groomed the monkey's face, neck, and head with his hand. To test whether the discrimination behavior depended on the shape of the stimuli or on the position of the pattern, these experimental parameters were changed in the different tasks. When the square pattern was assigned as correct and presented on the animal's left side, the average score for correct discrimination was 90% in the last 10 sessions out of 30 sessions, and this was statistically significant at a confidence level of p < 0.005 (Grant's table). Correct discrimination was statistically significant when the position of the square was randomly changed to the right and left side of the monkey, and also when the correct pattern was reversed from the square to the cross and its position was again randomly changed. Therefore, it was concluded that the grooming that an experimenter gives to a monkey can be applied as a positive reinforcer in operant conditioning. This experimental paradigm is considered to be useful for neurophysiological analysis of brain mechanisms underlying reward derived from somatosensory input in nonhuman primates.

Animals

Responses of primate taste cortex neurons to the astringent tastant tannic acid.

In order to advance knowledge of the neural control of feeding, we investigated the cortical representation of the taste of tannic acid, which produces the taste of astringency. It is a dietary component of biological importance particularly to arboreal primates. Recordings were made from 74 taste responsive neurons in the orbitofrontal cortex. Single neurons were found that were tuned to respond to 0.001 M tannic acid, and represented a subpopulation of neurons that was distinct from neurons responsive to the tastes of glucose (sweet), NaCl (salty), HCl (sour), quinine (bitter) and monosodium glutamate (umami). In addition, across the population of 74 neurons, tannic acid was as well represented as the tastes of NaCl, HCl quinine or monosodium glutamate. Multidimensional scaling analysis of the neuronal responses to the tastants indicates that tannic acid lies outside the boundaries of the four conventional taste qualities (sweet, sour, bitter and salty). Taken together these data indicate that the astringent taste of tannic acid should be considered as a taste quality, which receives a separate representation from sweet, salt, bitter and sour in the primate cortical taste areas.

Animals

Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task.

1. The primate orbitofrontal cortex receives inputs from the primary olfactory (pyriform) cortex and also from the primary taste cortex. To investigate how olfactory information is encoded in the orbitofrontal cortex, the responses of single neurons in the orbitofrontal cortex and surrounding areas were recorded during the performance of an olfactory discrimination task. In the task, the delivery of one of eight different odors indicated that the monkey could lick to obtain a taste of sucrose. If one of two other odors was delivered from the olfactometer, the monkey had to refrain from licking, otherwise he received a taste of saline. 2. Of the 1,580 neurons recorded in the orbitofrontal cortex, 3.1% (48) had olfactory responses and 34 (2.2%) responded differently to the different odors in the task. The neurons responded with a typical latency of 180 ms from the onset of odorant delivery. 3. Of the olfactory neurons with differential responses in the task, 35% responded solely on the basis of the taste reward association of the odorants. Such neurons responded either to all the rewarded stimuli, and none of the saline-associated stimuli, or vice versa. 4. The remaining 65% of these neurons showed differential selectivity for the stimuli based on the odor quality and not on the taste reward association of the odor. 5. The findings show that the olfactory representation within the orbitofrontal cortex reflects for some neurons (65%) which odor is present independently of its association with taste reward, and that for other neurons (35%), the olfactory response reflects (and encodes) the taste association of the odor. The additional finding that some of the odor-responsive neurons were also responsive to taste stimuli supports the hypothesis that odor-taste association learning at the level of single neurons in the orbitofrontal cortex enables such cells to show olfactory responses that reflect the taste association of the odor.

Analysis of Variance

Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex.

1. The primate orbitofrontal cortex is the site of convergence of information from primary taste and primary olfactory cortical regions. In addition, it receives projections from temporal lobe visual areas concerned with the representation of objects such as foods. Previous work has shown that the responses of gustatory neurons in the secondary taste area within the orbitofrontal cortex are modulated by hunger and satiety, in that they stop responding to the taste of a food on which an animal has been fed to behavioral satiation, yet may continue to respond to the taste of other foods. 2. This study demonstrates a similar modulation of the responses of olfactory and visual orbitofrontal cortex neurons after feeding to satiety. Seven of nine olfactory neurons that were responsive to the odors of foods, such as blackcurrant juice, were found to decrease their responses to the odor of the satiating food in a selective and statistically significant manner. 3. It also was found for eight of nine neurons that had selective responses to the sight of food, that they demonstrated a sensory-specific reduction in their visual responses to foods after satiation. 4. The responses of orbitofrontal cortex neurons selective for foods in more than one modality also were analyzed before and after feeding to satiation. Satiety often affected the responses of these multimodal neurons across all modalities, but a sensory-specific effect was not always demonstrable for both modalities. 5. These findings show that the olfactory and visual representations of food, as well as the taste representation of food, in the primate orbitofrontal cortex are modulated by hunger. Usually a component related to sensory-specific satiety can be demonstrated. The findings link at least part of the processing of olfactory and visual information in this brain region to the control of feeding-related behavior.

Analysis of Variance

Orbitofrontal cortex neurons: role in olfactory and visual association learning.

1. The orbitofrontal cortex is implicated in the rapid learning of new associations between visual stimuli and primary reinforcers such as taste. It is also the site of convergence of information from olfactory, gustatory, and visual modalities. To investigate the neuronal mechanisms underlying the formation of odor-taste associations, we made recordings from olfactory neurons in the orbitofrontal cortex during the performance of an olfactory discrimination task and its reversal in macaques. 2. It was found that 68% of odor-responsive neurons modified their responses after the changes in the taste reward associations of the odorants. Full reversal of the neuronal responses was seen in 25% of these neurons. Extinction of the differential neuronal responses after task reversal was seen in 43% of these neurons. 3. For comparison, visually responsive orbitofrontal neurons were tested during reversal of a visual discrimination task. Seventy-one percent of these visual cells showed rapid full reversal of the visual stimulus to which they responded, when the association of the visual with taste was reversed in the reversal task. 4. These demonstrate that of many orbitofrontal cortex olfactory neurons on the taste with which the odor is associated. 5. This modification is likely to be important for setting the motivational value of olfactory for feeding and other rewarded behavior. However, it is less complete, and much slower, than the modifications found or orbit frontal visual during visual-taste reversal. This relative inflexibility of olfactory responses is consistent with the need for some stability is odor-taste associations to facilitate the formation and perception of flavors.

Acoustic Stimulation

Representation of olfactory information in the primate orbitofrontal cortex.

1. To analyze the information represented about individual odor stimuli in the responses of single olfactory neurons in the primate orbitofrontal area, neuronal responses were measured to a set of seven to nine odorants in macaques performing an olfactory discrimination task. The population of neurons analyzed had responses that were significantly differential to the odorants. 2. Information theoretic analyses were applied to the responses of the neurons, and information measures were calculated from the firing rate of the responses and from the principal components of the responses. The information reflected by the firing rate of the response accounted for the majority of the information present (86%) when compared with the information derived from the first three principal components of the spike train. This indicated that temporal encoding had a very minor role in the encoding of olfactory information by single orbitofrontal olfactory cells. 3. The average information about which odorant was presented, averaged across the 38 neurons, was 0.09 bits, a figure that is low when compared with the information values previously published for the responses of temporal lobe face-selective neurons. 4. Application of information theoretic analyses to the responses of these neurons showed how much information about which stimulus was delivered was present in the responses of individual neurons. It was found that for the majority of the neurons significant amounts of information were reflected about one or two of the odorants presented. 5. For each neuron, the information reflected in the responses of that neuron about the reinforcement value and the information about the identity of the odorants were calculated. It is shown that many neurons carry information about which of the odorants was presented; in addition, some neurons reflect information only about the taste association of the stimuli and not about odorant identity. 6. Measurements of the sparseness of the representation indicated that a broadly distributed representation of the identity of odorants was present in this population of neurons.

Animals

Learning mechanisms in the temporal lobe visual cortex.

Neurophysiological experiments are described which show that neurons form ensemble encoded representations of stimuli such as faces which are relatively invariant with respect to size, contrast, spatial frequency, translation, and view. It is shown that new representations of objects can be formed with less than 5 s of visual experience with those objects. Mechanisms by which the brain could perform this invariant recognition, and learn the representations required for recognition, are described. A neural network simulation of these mechanisms for learning invariant representations is then described. The model uses a multistage feed-forward architecture, and is able to learn invariant representations of objects including faces by use of a Hebbian synaptic modification rule which incorporates a short memory trace (0.5 s) of preceding activity. This trace rule enables the network to learn the properties of objects which are spatio-temporally invariant over this time scale.

Animals

View-responsive neurons in the primate hippocampal complex.

Recordings were made from single neurons in the hippocampus and parahippocampal gyrus while macaques were moved on a platform mounted on a free-moving robot or on wheels in a cue-controlled 2 m x 2 m x 2 m environment, in order to investigate the representation of space and of spatial memory in the primate hippocampus. The test conditions allowed factors that might account for spatial firing of the cells, including the spatial location where the monkey looked, the place were the monkey was, and the head direction of the monkey, to be identified. The responses of some ("view") neurons depended on where the monkey was looking in the environment, but not on the place of the monkey in the environment. The responses of one other neuron depended on a combination of where the monkey was facing and his place in the test chamber. The response of view-dependent neurons was affected by occlusion of the visual field. It was possible to show for one neuron that its "view" response rotated with rotation of the test chamber. Some neurons responded to a combination of whole-body motion and view or place, and one neuron responded in relation to whole-body movement to a particular place. One neuron responded depending on the place where the monkey was in the environment and relatively independently of view. The representations of space provided by hippocampal view-responsive neurons may be useful in forming memories of spatial environments (for example, of where an object has been seen and of where the monkey is as defined by seen views) and, together with whole-body motion cells, in remembering trajectories through environments, which is of use, for example, in short range spatial navigation.

Animals

The responses of single neurons in the temporal visual cortical areas of the macaque when more than one stimulus is present in the receptive field.

Neurons in the temporal visual cortical areas of primates have large receptive fields, which can show considerable selectivity for what the stimulus is irrespective of exactly where it is in the visual field. This is called translation invariance. However, such results have been found when there is only one stimulus in the visual field. The question arises of how the visual system operates in a cluttered environment. To investigate this we measured the responses of neurons with face-selective responses in the cortex in the anterior part of the superior temporal sulcus of rhesus macaques performing a visual fixation task. We found that the response of neurons to an effective face centred 8.5 degrees from the fovea was decreased to 71% if an ineffective face stimulus for that cell was present at the fovea. In a similar way, introduction of a parafoveal ineffective face stimulus decreased the responses of these neurons to an effective face stimulus at the fovea to 75%. In addition to these interactions, it was found that an effective stimulus object at the fovea produced a larger response than when it was parafoveal, and that this weighting towards an object at the fovea was also seen when more than one object was present in the visual field. The implication of this weighting of the responses of neurons towards objects at the fovea, even in an environment with more than one object present, is that the output of the visual system provides information to subsequent systems particularly about objects at the fovea, so that learning about these objects (and less about other objects elsewhere in the visual field) is facilitated.

Animals

Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate.

A cortical taste region has recently been identified in the caudolateral orbitofrontal cortex of the macaque. The afferents to this region were investigated by means of retrograde tracing, using six injections of wheatgerm-conjugated horseradish peroxidase. The area of taste cortex was first identified physiologically in all the monkeys used in this anatomical study. The four injections into the middle and posterior part of this region resulted in large numbers of labelled cell bodies in the insular-opercular primary taste cortex. Following the two more anterior injections, label was found predominantly in the caudal part of the cardolateral orbitofrontal cortex itself. None of the injections resulted in labelled cells in the gustatory thalamic nucleus ventralis posterior medialis, pars parvocellularis, although all injections resulted in label of the mediodorsal nucleus of the thalamus. Afferents were also seen from more anterior parts of the orbitofrontal taste cortex, which may represent backprojections from subsequent taste areas. These results suggest that the caudolateral orbitofrontal cortex contains a higher-order taste cortex.

Amygdala

Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex.

1. To analyze the selectivity and the sparseness of firing to visual stimuli of single neurons in the primate temporal cortical visual area, neuronal responses were measured to a set of 68 visual stimuli in macaques performing a visual fixation task. The population of neurons analyzed had responses that occurred primarily to faces. The stimuli included 23 faces, and 45 nonface images of real-world scenes, so that the function of this brain region could be analyzed when it was processing natural scenes. 2. The neurons were selected to meet the previously used criteria of face selectivity by responding more than twice as much to the optimal face as to the optimal nonface stimulus in the set. Application of information theoretic analyses to the responses of these neurons confirmed that their responses contained much more information about which of 20 face stimuli had been seen (on average 0.4 bits) than about which (of 20) nonface stimuli had been seen (on average 0.07 bits). 3. The sparseness of the representation of a scene or object provided by each of these neurons (which can be thought of as the proportion of stimuli to which the neuron responds, and which is fundamental to understanding the network operation of the system) can be defined as [formula: see text] where ri is the firing rate to the ith stimulus in the set of n stimuli. The sparseness has a maximal value of 1.0. It was found that the sparseness of the representation of the 68 stimuli by each neuron had an average across all neurons of 0.65. This indicates a rather distributed representation. 4. If the spontaneous firing rate was subtracted from the firing rate of the neuron to each stimulus, so that the changes of firing rate, i.e., the responses of the neurons, were used in the sparseness calculation, then the "response sparseness" had a lower value, with a mean of 0.33 for the population of neurons, or 0.60 if calculated over the set of faces. 5. Multidimensional scaling to produce a stimulus space represented by this population of neurons showed that the different faces were well separated in the space created, whereas the different nonface stimuli were grouped together in the space. 6. The information analyses and multidimensional scaling provided evidence that what was made explicit in the responses of these neurons was information about which face had been seen.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Brain mechanisms of satiety and taste in macaques.

Flavor is the primary reinforcer of eating. As satiety is induced, the reinforcement of flavor is lost. Since flavor derives largely from taste, one might expect gustatory responsiveness to decline with increasing satiety. However, no such loss of sensitivity occurs in humans, even as the reinforcing value of taste declines with satiety. Thus, we explored the effect of satiety on taste responses at several levels of the macaque's nervous system to determine where is influence began. Taste-evoked activity in the NTS and primary taste cortex was unaffected by the induction of satiety through or administration of glucose. Taste cortex projects to amygdala and orbitofrontal cortex (OFC). In amygdala, satiety reduced responsiveness by 58%; in OFC, neurons were fully suppressed. Both amygdala and OFC project to the hypothalamus, where taste responsiveness was also suppressed. Thus, the neural impact of food is reduced not in area devoted to quality analysis, but in those concerned with motivation and reinforcement.

Administration, Oral

Processing speed in the cerebral cortex and the neurophysiology of visual masking.

In experiments to investigate the duration of the time for which cortical neurons respond when the identification of a visual stimulus is just possible, we presented a test face stimulus for 16 ms, and followed it at different intervals by a masking stimulus (either an N-O pattern or a face) while recording from single neurons in the temporal visual cortex of macaques. When there was no mask the cells responded to the 16 ms of the test stimulus for 200-300 ms, far longer than the presentation time. We suggest that this reflects the operation of a short-term memory system implemented in cortical circuitry. If the mask was a stimulus which did not stimulate the cells (either a non-face pattern or a face which was a non-effective stimulus for that cell), then, as the interval between the onset of the test stimulus and the onset of the mask stimulus (the stimulus onset asynchrony) was reduced, the length of time for which the cells fired in response to the test stimulus was reduced. It is suggested that this is due to the mask stimulating adjacent cells in the cortex which by lateral inhibition reduce the responses of the cells activated by the test stimulus. When the stimulus onset asynchrony was 20 ms, face-selective neurons in the inferior temporal cortex of macaques responded for a period of 20-30 ms before their firing was interrupted by the mask. With the same test-mask stimulus onset asynchrony of 20 ms, humans could just identify which of six faces was shown.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals

Computational analysis of the role of the hippocampus in memory.

The authors draw together the results of a series of detailed computational studies and show how they are contributing to the development of a theory of hippocampal function. A new part of the theory introduced here is a quantitative analysis of how backprojections from the hippocampus to the neocortex could lead to the recall of recent memories. The theory is then compared with other theories of hippocampal function. First, what is computed by the hippocampus is considered. The hypothesis the authors advocate, on the basis of the effects of damage to the hippocampus and neuronal activity recorded in it, is that it is involved in the formation of new memories by acting as an intermediate-term buffer store for information about episodes, particularly for spatial, but probably also for some nonspatial, information. The authors analyze how the hippocampus could perform this function, by producing a computational theory of how it operates, based on neuroanatomical and neurophysiological information about the different neuronal systems contained within the hippocampus. Key hypotheses are that the CA3 pyramidal cells operate as a single autoassociation network to store new episodic information as it arrives via a number of specialized preprocessing stages from many association areas of the cerebral cortex, and that the dentate granule cell/mossy fiber system is important, particularly during learning, to help to produce a new pattern of firing in the CA3 cells for each episode. The computational analysis shows how many memories could be stored in the hippocampus and how quickly the CA3 autoassociation system would operate during recall. The analysis is then extended to show how the CA3 system could be used to recall a whole episodic memory when only a fragment of it is presented. It is shown how this recall could operate using modified synapses in backprojection pathways from the hippocampus to the cerebral neocortex, resulting in reinstatement of neuronal activity in association areas of the cerebral neocortex similar to that present during the original episode. The recalled information in the cerebral neocortex could then be used by the neocortex in the formation of long-term memories.

Animals

The responses of neurons in the temporal cortex of primates, and face identification and detection.

The ability of a human observer to detect the presence of a briefly flashed picture of a face can depend on the picture's spatial configuration, that is on whether its features are rearranged (jumbled) or are in their normal configuration. The face-detection effect (FDE) is found under conditions of backward masking, when the presence of a face can be detected with shorter masking intervals when it is in the normal than when in the rear-ranged configuration. A similar effect is found when the subject is asked to classify the face as rearranged or not - the face-classification effect (FCE). Part of the interest of the FDE and the FCE is that they show how the configuration of a stimulus can be an important factor in the perceptual processing which leads to detection and classification of the stimulus. To analyse these effects we recorded from single neurons in the cortex in the superior temporal sulcus of macaques when they were shown (in a visual fixation task) normal and rearranged faces under backward masking conditions shown in experiments 2 and 3 to produce, with the same apparatus, the FCE, and also to produce comparable effects on the identification of which face was present (called hereafter the face-identification effect), and also of the clarity of the face. We found in experiment 1 that there are some face-selective neurons which respond to faces only, or better, when the features in the faces are in their normal configuration rather than rearranged. We also showed in this experiment that the difference in the response to the normal as compared to the rearranged faces became greater when the masking stimulus was delayed more. Thus, at intermediate delays, there are more neurons active for the normal than for the rearranged face. We therefore propose that the FDE, the FCE, and the face-identification effect arise because the total number of neurons activated by faces in their normal configuration is greater than that activated by rearranged faces, because of the sensitivity of some face-selective neurons to the spatial arrangement of the features. The experiments also show that backward visual masking does produce abrupt termination of the firing of neurons in the temporal cortical visual system, so that the duration of a neuronal response is very short when visual stimuli can just be perceived.

Analysis of Variance

Neural networks in the brain involved in memory and recall.

We have considered how the neuronal network architecture of the hippocampus may enable it to act as an intermediate term buffer store for recent memories, and how information may be recalled from it to the cerebral cortex using modified synapses in back-projection pathways from the hippocampus to the cerebral cortex. The recalled information in the cerebral neocortex could then be used by the neocortex in the formation of long-term memories, which is severely impaired by damage to the hippocampus.

Animals

Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage.

A group of patients with damage to the ventral part of the frontal lobes was severely impaired relative to a group of patients without damage in this area (the non-ventral group) in the reversal and in the extinction of simple visual discrimination tests. In these tests they continued to make responses to a previously rewarded stimulus. Patients often reported verbally that the contingencies had changed, but were unable to alter their behaviour appropriately. These impairments occurred independently of IQ or verbal memory impairments. The perseverative touching of a previously rewarded stimulus is consistent with work with non-human primates showing impaired reversal and extinction after orbitofrontal lesions. Performance on these reversal and extinction tests was highly correlated with scores obtained on a behaviour questionnaire, which reflected the degree of disinhibited and socially inappropriate behaviour exhibited by patients. It is suggested that a difficulty in modifying responses, especially when followed by negative consequences, as manifested in these simple laboratory tests, may contribute to the inappropriate behaviour shown in daily life by patients with frontal lobe damage.

Activities of Daily Living