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E T Rolls

Publications and source records attributed to E T Rolls.

At least 91 records · Page 5Linked to original sources

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↗

Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque.

1. The responses of single neurons in the inferior temporal cortex and the cortex in the banks of the anterior part of the superior temporal sulcus of three awake, behaving macaques were recorded during a visual fixation task. Stimulus images subtending 17 or 8.5 degrees were presented in the center of the display area, and fixation was either at the center of the display area, or at one of four positions that were on the stimulus, or several degrees off the edge of the test stimulus. The experiments were performed with face-selective cells, and the responses were compared for fixation at each position for both effective and noneffective face stimuli for each cell. 2. The firing rates of most neurons to an effective image did not significantly alter when visual fixation was as far eccentric as the edge of the face, and they showed only a small reduction when the fixation point was up to 4 degrees from the edge of the face. Moreover, stimulus selectivity across faces was maintained throughout this region of the visual field. 3. The centers of the receptive fields of the cells, as shown by the calculated "centers of gravity," were close to the fovea, with almost all being within 3 degrees of the fovea. 4. The receptive fields of the cells typically crossed the vertical midline for at least 5 degrees. 5. Information theory procedures were used to analyze the spike trains of the visual neurons. Nearly six times more information was carried by these neurons' firing rate about the identity of an image than about its position in the visual field. Thus the information theory analysis showed that the responses of these neurons reflected information about which stimulus had been seen in a relatively translation invariant way. 6. Principal component analysis showed that principal component 1 (PC1) is related primarily to firing rate and reflected information primarily about stimulus identity. (For identity PC2 added only 14% more information to that contained in PC1.) Principal component 2 (PC2) was more closely related to neuronal response latencies, which increased with increasing eccentricity of the image in the visual field. PC2 reflected information about the position of the stimulus in the visual field, in that PC2 added 109% more information to that contained in PC1 about the position of the stimulus in the visual field.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Neurons responding to whole-body motion in the primate hippocampus.

We describe here hippocampal cells that respond during whole-body motion when a monkey is moved on a remote-controlled robot-mounted platform in a cue-controlled test chamber (2 x 2 x 2 m). Some of these cells responded to linear motion, and others to axial rotation. Some of these cells responded when the same motion occurred without a view of the visual field. Such cells appeared to be driven by vestibular inputs. Other cells required a view of the visual field for their response, and these cells appeared to be driven by the visual motion relative to the monkey of the test chamber. Further evidence that this was the case was that some of the cells responded to rotation and linear motion of the test chamber while the monkey remained stationary. Other cells responded to combinations of whole-body motion and a view of the environment. These findings show that information about whole-body motion, as well as about where the animal is looking in an environment, is represented in the primate hippocampus. We suggest that this information is important in spatial memory and thus in spatial navigation.

Animals↗

Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex.

Behavioral and perceptual responses to food depend on a convergence between gustatory, olfactory, and visual information. In previous studies a secondary cortical taste area has been found in the caudolateral orbitofrontal cortex of the primate. Furthermore, neurons with olfactory responses have been recorded in a more medial part of the orbitofrontal cortex, and visual inputs have been shown to influence neurons in an intermediate region. These studies suggest that the orbitofrontal cortex may act as a region for convergence of multiple sensory modalities including chemosensation. In the present study neurons throughout the caudal two-thirds of the orbitofrontal cortex of the macaque were tested to gustatory, to olfactory, and to visual stimulation to investigate whether convergence occurs. Neurons in this region of cortex were found that responded to stimulation of the taste, olfactory, or visual system. In addition, some neurons were found with bimodal responses, responding for example to both taste and olfactory, or taste and visual stimuli. Since these multimodal neurons were found in very close proximity to unimodal neurons, and the unimodal sensory neurons were intermingled, it is possible that the orbitofrontal cortex represents the first cortical area of convergence for these three modalities in primates.

Acoustic Stimulation↗

Neuronal responses in the ventral striatum of the behaving macaque.

To analyse the functioning of the ventral striatum, the responses of more than 1,000 single neurons were recorded in a region which included the nucleus accumbens and olfactory tubercle in 5 macaque monkeys. While the monkeys performed visual discrimination and related feeding tasks, the different populations of neurons found included neurons which responded to novel visual stimuli; to reinforcement-related visual stimuli such as (for different neurons) food-related stimuli, aversive stimuli, or faces; to other visual stimuli; in relation to somatosensory stimulation and movement; or to cues which signalled the start of a task. The neurons with responses to reinforcing or novel visual stimuli may reflect the inputs to the ventral striatum from the amygdala and hippocampus, and are consistent with the hypothesis that the ventral striatum provides a route for learned reinforcing and novel visual stimuli to influence behaviour.

Amygdala↗

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.

Action Potentials↗

Responses of single neurons in the hippocampus of the macaque related to recognition memory.

In order to analyse how hippocampal activity is related to memory, the activity of single hippocampal neurons was recorded while macaques performed a recognition memory task. In the task, the first time a stimulus was shown, no reward could be obtained, and the second time a visual stimulus was shown, the monkeys could lick to obtain fruit juice. Many other stimuli could intervene between the novel and familiar presentations of each stimulus. Of 660 neurons analysed, 15 (2.3%) responded differently to novel and to familiar stimuli, with the majority of these responding more to novel than to familiar stimuli. The latencies of the differential responses of the neurons were typically in the range 140-260 ms. The responses of these neurons reflected whether a visual stimulus had been seen recently, in that the neurons responded differently to novel and familiar presentations of a stimulus when a median of 21 other stimuli intervened between the novel and familiar presentations. The responses of these neurons were shown to be related to whether the stimuli had been seen before, not to the reinforcement or the lick responses made, in that the neurons did not have comparable responses in a visual discrimination task in which licks were made to a rewarding stimulus but not to another stimulus. It is concluded that the activity of a small but significant proportion of hippocampal neurons is related to whether a stimulus has been seen before recently, and that this processing is likely to be involved in memory.

Animals↗

The effects of stimulus novelty and familiarity on neuronal activity in the amygdala of monkeys performing recognition memory tasks.

The function of the amygdala in behavioural responses to novel stimuli and its possible function in recognition memory were investigated by recording the responses of 659 amygdaloid neurons in monkeys performing recognition memory and visual discrimination tasks. The aim was to determine the contribution of the amygdala in the encoding of familiarity and therefore its role in supporting memory-related neuronal mechanisms in the basal forebrain. The responses of three groups of neurons reflected different forms of memory. One group (n = 10) responded maximally to novel stimuli and significantly less so to the same stimuli when they were familiar. The calculated memory spans of these neurons were in the range of 2-10 intervening trials, and this short-term retention of information may reflect the operation of a neural mechanism encoding memory for the recency of stimulus presentation. Two other groups responded to the sight of particular categories of familiar stimuli: to foods (n = 6) or to faces (n = 10). The responses of some of these stimulus-selective neurons declined with repeated presentations of foods (3/4 tests) and faces (2/6 tests). The activity of these latter two groups of neurons may be involved in behavioural responses to familiar visual stimuli, particularly when such stimuli have affective or motivational significance. We conclude that the neurophysiological data provide evidence of amygdaloid mechanisms for the recognition of recently seen visual stimuli. However, these amygdaloid mechanisms do not appear to be sufficient to support the performance of long-term recognition memory tasks without additional and complementary functions carried out by other ventromedial temporal, prefrontal and diencephalic structures which also project to the basal forebrain.

Amygdala↗

Information encoding and the responses of single neurons in the primate temporal visual cortex.

1. The possibility of temporal encoding in the spike trains of single neurons recorded in the temporal lobe visual cortical areas of rhesus macaques was analyzed with the use of principal component and information theory analyses of smoothed spike trains. The neurons analyzed had responses selective for faces. 2. Provided that a correction was applied to earlier methods of principal component analysis used for neuronal spike trains, it was shown that the first principal component provides by a great extent the most information, with the second and third adding only small proportions (on average 18.8 and 8.4%, respectively). 3. It was shown that the magnitude of the second and higher principal components is even smaller if the spike train analysis is started after the onset of the neuronal response, instead of before the neuronal response has started. This suggests that variations in response latency are at least a part of what is reflected by the second and higher principal components. 4. The first principal component was correlated with the mean firing rate of the neurons. The second and higher principal components reflected at least partly the onset properties of the neuronal responses, such as response latency differences between the stimuli. 5. A considerable proportion of the information available from principal components 1-3 is available in the firing rate of the neuron. 6. Periods of the firing rate of as little as 50 or even 20 ms are sufficient to give a reasonable estimate of the firing rate of the neuron. 7. Information theory analysis showed that in short epochs (e.g., 50 ms) the information available from the firing rate can be as high, on average, as 84.4% of that available from the firing rate calculated over 400 ms, and 52.0% of that available from principal components 1-3 in the 400-ms period. It was also found that 44.0% of the information calculated from the first three principal components is available in the firing rates calculated over epochs as short as 20 ms. 8. More information was available near the start of the neuronal response, and the information available from short epochs became less later in the neuronal response. 9. Taken together, these analyses provide evidence that a short period of firing taken close to the start of the neuronal response provides a reasonable proportion of the total information that would be available if a long period of neuronal firing (e.g., 400 ms) were utilized to extract it, even if temporal encoding were used.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗