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E T Rolls

Publications and source records attributed to E T Rolls.

At least 73 records · Page 4Linked to original sources

The representational capacity of the distributed encoding of information provided by populations of neurons in primate temporal visual cortex.

It has been shown that it is possible to read, from the firing rates of just a small population of neurons, the code that is used in the macaque temporal lobe visual cortex to distinguish between different faces being looked at. To analyse the information provided by populations of single neurons in the primate temporal cortical visual areas, the responses of a population of 14 neurons to 20 visual stimuli were analysed in a macaque performing a visual fixation task. The population of neurons analysed responded primarily to faces, and the stimuli utilised were all human and monkey faces. Each neuron had its own response profile to the different members of the stimulus set. The mean response of each neuron to each stimulus in the set was calculated from a fraction of the ten trials of data available for every stimulus. From the remaining data, it was possible to calculate, for any population response vector, the relative likelihoods that it had been elicited by each of the stimuli in the set. By comparison with the stimuli actually shown, the mean percentage correct identification was computed and also the mean information about the stimuli, in bits, that the population of neurons carried on a single trial. When the decoding algorithm used for this calculation approximated an optimal, Bayesian estimate of the relative likelihoods, the percentage correct increased from 14% correct (chance was 5% correct) with one neuron to 67% with 14 neurons. The information conveyed by the population of neurons increased approximately linearly from 0.33 bits with one neuron to 2.77 bits with 14 neurons. This leads to the important conclusion that the number of stimuli that can be encoded by a population of neurons in this part of the visual system increases approximately exponentially as the number of cells in the sample increases (in that the log of the number of stimuli increases almost linearly). This is in contrast to a local encoding scheme (of "grandmother" cells), in which the number of stimuli encoded increases linearly with the number of cells in the sample. Thus one of the potentially important properties of distributed representations, an exponential increase in the number of stimuli that can be represented, has been demonstrated in the brain with this population of neurons. When the algorithm used for estimating stimulus likelihood was as simple as could be easily implemented by neurons receiving the population's output (based on just the dot product between the population response vector and each mean response vector), it was still found that the 14-neuron population produced 66% correct guesses and conveyed 2.30 bits of information, or 83% of the information that could be extracted with the nearly optimal procedure. It was also shown that, although there was some redundancy in the representation (with each neuron contributing to the information carried by the whole population 60% of the information it carried alone, rather than 100%), this is due to the fact that the number of stimuli in the set was limited (it was 20). The data are consistent with minimal redundancy for sufficiently large and diverse sets of stimuli. The implication for brain connectivity of the distributed encoding scheme, which was demonstrated here in the case of faces, is that a neuron can receive a great deal of information about what is encoded by a large population of neurons if it is able to receive its inputs from a random subset of these neurons, even of limited numbers (e.g. hundreds).

Algorithms↗

Olfactory sensory-specific satiety in humans.

It is shown that olfactory sensory-specific satiety, measured by ratings of the pleasantness of the odour of a food eaten relative to the change in pleasantness of other foods, can be produced by eating a food to satiety. It is also shown that olfactory and taste sensory-specific satiety can be produced by chewing samples of a food for approximately as long as the food would normally be eaten in a meal. It is further shown that partial olfactory sensory-specific satiety can be produced by smelling the food for approximately as long as it would be in the mouth during a meal. These sensory-specific changes in the pleasantness of a food do not appear to reflect changes in the intensity of the foods, which were small and not highly correlated with the changes in pleasantness. The results show that at least partial olfactory, as well as taste, sensory-specific satiety does not require food to enter the gastrointestinal system, and does not depend on the ingestion of calories. The implications for the control of food intake, and the way in which the brain computes sensory-specific satiety, are considered.

Adult↗

Invariant face and object recognition in the visual system.

Neurophysiological evidence is described, showing that some neurons in the macaque temporal cortical visual areas have responses that are invariant with respect to the position, size and view of faces and objects, and that these neurons show rapid processing and rapid learning. A theory is then described of how such invariant representations may be produced in a hierarchically organized set of visual cortical areas with convergent connectivity. The theory proposes that neurons in these visual areas use a modified Hebb synaptic modification rule with a short-term memory trace to capture whatever can be captured at each stage that is invariant about objects as the object changes in retinal position, size, rotation and view. Simulations are then described which explore the operation of the architecture. The simulations show that such a processing system can build invariant representations of objects.

Animals↗

Information in the neuronal representation of individual stimuli in the primate temporal visual cortex.

To analyze the information provided about individual visual stimuli in the responses of single neurons in the primate temporal lobe visual cortex, neuronal responses to a set of 65 visual stimuli were recorded in macaques performing a visual fixation task and analyzed using information theoretical measures. The population of neurons analyzed responded primarily to faces. The stimuli included 23 faces and 42 nonface images of real-world scenes, so that the function of this brain region could be analyzed when it was processing relatively natural scenes. It was found that for the majority of the neurons significant amounts of information were reflected about which of several of the 23 faces had been seen. Thus the representation was not local, for in a local representation almost all the information available can be obtained when the single stimulus to which the neuron responds best is shown. It is shown that the information available about any one stimulus depended on how different (for example, how many standard deviations) the response to that stimulus was from the average response to all stimuli. This was the case for responses below the average response as well as above. It is shown that the fraction of information carried by the low firing rates of a cell was large--much larger than that carried by the high firing rates. Part of the reason for this is that the probability distribution of different firing rates is biased toward low values (though with fewer very low values than would be predicted by an exponential distribution). Another factor is that the variability of the response is large at intermediate and high firing rates. Another finding is that at short sampling intervals (such as 20 ms) the neurons code information efficiently, by effectively acting as binary variables and behaving less noisily than would be expected of a Poisson process.

Action Potentials↗

Spatial view cells in the primate hippocampus.

Hippocampal function was analysed by making recordings in rhesus monkeys actively walking in the laboratory. In a sample of 352 cells recorded in the hippocampus and parahippocampal cortex, a population of 'spatial view' cells was found to respond when the monkey looked at a part of the environment. The responses of these hippocampal neurons (i) occur to a view of space 'out there', not to the place where the monkey is, (ii) depend on where the monkey is looking, as shown by measuring eye position, (iii) do not encode head direction, and (iv) provide a spatial representation that is allocentric, i.e. in world coordinates. This representation of space 'out there' would be an appropriate part of a primate memory system involved in memories of where in an environment an object was seen, and more generally in the memory of particular events or episodes for which a spatial component normally provides part of the context.

Animals↗

Taste and olfactory processing in the brain and its relation to the control of eating.

Taste processing in primates through the nucleus of the solitary tract and the primary taste cortex is shown to represent the identity and intensity of taste inputs. In contrast, in the secondary taste cortex in the orbitofrontal area, single neurons respond to the taste of a food only if hunger is present. The neurons here reflect the reward value of taste. They show sensory-specific satiety. In addition to neurons with best responses to sweet, salt, bitter, and sour, there are separate representations of the taste of protein ("umami") and of astringency (e.g., tannic acid). In the orbitofrontal cortex, olfactory inputs converge onto neurons with taste inputs, forming representations of flavor. Neurons in this region may also respond to the sight of food and to its texture. The olfactory representation for some neurons reflects the taste association of odors; and olfactory sensory-specific satiety is represented in this part of the brain. Rapid learning of visual-to-taste associations is also a feature of the neural processing that occurs in the orbitofrontal cortex.

Animals↗

Rapid visual learning in neurones of the primate temporal visual cortex.

The human visual system can learn to recognize visual stimuli rapidly. For example, humans can accurately reconstruct meaningful objects out of fragmentary evidence, once they have seen the same object in its unambiguous form. The anterior temporal cortical areas of macaques contain some neurones with invariant visual responses which appear to provide a representation of complex patterns and objects, such as faces. Remarkably, these neurones show an enhancement of response after brief (e.g. 5 s) exposure to the unambiguous stimulus, an effect that appears to reflect the neural basis of the rapid perceptual learning seen in humans.

Animals↗

The orbitofrontal cortex.

The orbitofrontal cortex contains the secondary taste cortex, in which the reward value of taste is represented. It also contains the secondary and tertiary olfactory cortical areas, in which information about the identity and also about the reward value of odours is represented. The orbitofrontal cortex also receives information about the sight of objects from the temporal lobe cortical visual areas, and is involved in learning and in reversing stimulus-reinforcement associations. The stimulus might be a visual or olfactory stimulus, and the primary (unlearned) reinforcer a taste or touch. Damage to the orbitofrontal cortex impairs the learning and reversal of stimulus-reinforcement associations, and thus the correction of behavioural responses when these are no longer appropriate because previous reinforcement contingencies change. The information which reaches the orbitofrontal cortex for these functions includes information about faces, and damage to the orbitofrontal cortex can impair face expression identification. This evidence thus shows that the orbitofrontal cortex is involved in decoding some primary reinforcers such as taste; in learning and reversing associations of visual and other stimuli to these primary reinforcers; and plays an executive function in controlling and correcting reward-related and punishment-related behaviour, and thus in emotion.

Amygdala↗

A theory of hippocampal function in memory.

First, what is computed by the hippocampus is considered. Based on the effects of damage to the hippocampus and neuronal activity recorded in the primate hippocampus, it is suggested that it is involved in associating together information usually originating from different cortical regions, for example, about objects and their place in a spatial environment. The rapid formation of such context-dependent memories is prototypical of memories of particular events or episodes. Second, a computational theory of how it performs this function, based on neuroanatomical and neurophysiological information about the different neuronal systems contained within the hippocampus, is described. 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 different 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 the whole of an episodic memory when only a fragment of it is presented. It is shown how this retrieval within the hippocampus could lead to recall of neuronal activity in association areas of the cerebral neocortex similar to that present during the original episode, via modified synapses in backprojection pathways from the hippocampus to the cerebral neocortex. The recalled information in the cerebral neocortex could then by used by the neocortex in the formation of long-term memories and/or in the selection of appropriate actions.

Amnesia, Retrograde↗

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↗

Speed, noise, information and the graded nature of neuronal responses.

How the firing rate of a neuron carries information depends on the time over which rates are measured. For very short times, the amount of information conveyed depends, in a universal way, on the mean rates only (trial-to-trial variability is irrelevant) and the cell response can be taken to be binary (although an ideal binary response would convey more). For longer times, noise as well as the graded nature of the response come into play, with opposite effects. Which times can be considered 'short' varies with the brain area considered and, possibly, with the processing speed it is required to operate at.

Journal Article↗

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↗