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Shape representation in the inferior temporal cortex of monkeys.

BACKGROUND: The inferior temporal cortex (IT) of the monkey has long been known to play an essential role in visual object recognition. Damage to this area results in severe deficits in perceptual learning and object recognition, without significantly affecting basic visual capacities. Consistent with these ablation studies is the discovery of IT neurons that respond to complex two-dimensional visual patterns, or objects such as faces or body parts. What is the role of these neurons in object recognition? Is such a complex configurational selectivity specific to biologically meaningful objects, or does it develop as a result of extensive exposure to any objects whose identification relies on subtle shape differences? If so, would IT neurons respond selectively to recently learned views of features of novel objects? The present study addresses this question by using combined psychophysical and electrophysiological experiments, in which monkeys learned to classify and recognize computer-generated three-dimensional objects. RESULTS: A population of IT neurons was found that responded selectively to views of previously unfamiliar objects. The cells discharged maximally to one view of an object, and their response declined gradually as the object was rotated away from this preferred view. No selective responses were ever encountered for views that the animal systematically failed to recognize. Most neurons also exhibited orientation-dependent responses during view-plane rotations. Some neurons were found to be tuned around two views of the same object, and a very small number of cells responded in a view-invariant manner. For the five different objects that were used extensively during the training of the animals, and for which behavioral performance became view-independent, multiple cells were found that were tuned around different views of the same object. A number of view-selective units showed response invariance for changes in the size of the object or the position of its image within the parafovea. CONCLUSION: Our results suggest that IT neurons can develop a complex receptive field organization as a consequence of extensive training in the discrimination and recognition of objects. None of these objects had any prior meaning for the animal, nor did they resemble anything familiar in the monkey's environment. Simple geometric features did not appear to account for the neurons' selective responses. These findings support the idea that a population of neurons--each tuned to a different object aspect, and each showing a certain degree of invariance to image transformations--may, as an ensemble, encode at least some types of complex three-dimensional objects. In such a system, several neurons may be active for any given vantage point, with a single unit acting like a blurred template for a limited neighborhood of a single view.

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Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding.

Previous analysis of the firing of individual rat hippocampal place cells has shown that their firing rate increases when they enter a place field and that their phase of firing relative to the ongoing theta oscillation (7-12 Hz) varies systematically as the rat traverses the place field, a phenomenon termed the theta phase precession. To study the relative contribution of phased-coded and rate-coded information, we reconstructed the animal's position on a linear track using spikes recorded simultaneously from 38 hippocampal neurons. Two previous studies of this kind found no evidence that phase information substantially improves reconstruction accuracy. We have found that reconstruction is improved provided epochs with large, systematic errors are first excluded. With this condition, use of both phase and rate information improves the reconstruction accuracy by >43% as compared with the use of rate information alone. Furthermore, it becomes possible to predict the rat's position on a 204-cm track with very high accuracy (error of <3 cm). The best reconstructions were obtained with more than three phase divisions per theta cycle. These results strengthen the hypothesis that information in rat hippocampal place cells is encoded by the phase of theta at which cells fire.

Action Potentials↗

Stimulus congruence and the Simon effect.

A standard experimental procedure was implemented with novel response requirements to assess the hypothesis that the Simon effect is attributable not to the irrelevant stimulus-response relationship, but to the congruence between stimulus attributes. The stimulus ensemble consisted of the words LEFT and RIGHT, one of which was presented on each trial to the left or right of a central fixation point. The distinctive feature of the task is that subjects were asked to respond, by laterally placed keys, whether or not the stimulus word was in accord (i. e., congruent) with its location on the display. Asking subjects to judge stimulus congruence directly enables the effect of congruence to be assessed, as well as independent estimates of the two irrelevant S-R relationships that apply in the task--that is, between the response location and (1) the stimulus location (the Simon effect) and (2) the stimulus word (the reverse Simon effect). Marked effects were obtained in all three cases. Stimulus congruence remains in contention as a factor in the explanation of the Simon effect, but the strong effects of irrelevant S-R factors suggest that a more comprehensive account of the Simon effect is needed. An explanation in terms of stimulus salience, based on an interactive activational model, is briefly discussed.

Adult↗

Sequential rearrangements of the ensemble activity of putamen neurons in the monkey brain as a correlate of continuous behavior.

Simultaneous recordings were made of the spike activity of groups of 6-7 neurons in the putamen in two monkeys (Macaca nemestrina and Macaca mulatta) during performance of alternative spatial selection. Discriminant analysis was used to evaluate the magnitude of rearrangements in spike activity in groups of neurons during transitions from each step of the behavioral program to the next, along with the degree of differences in reactivity mosaics formed at each step in different versions of task execution. Rearrangements in spike activity were noted at all steps of the program. The dynamics of rearrangements on selection of the right and left feeders were different, leading to the appearance of significant differences in the reactivity mosaics at the decision-taking and reinforcement-receiving steps. The rearrangements preceding voluntary movement of one hand were more marked in the contralateral hemisphere. During performance of movements, the volume of rearrangements could increase, though differences in rearrangements accompanying movements of the right and left hands decreased. On receipt of reinforcement, rearrangements were greater when the animals selected a specified feeder (the left feeder) independently of which hemisphere was recorded.

Action Potentials↗

Neural correlates of artificial syntactic structure classification.

The human brain supports acquisition mechanisms that extract structural regularities implicitly from experience without the induction of an explicit model. It has been argued that the capacity to generalize to new input is based on the acquisition of abstract representations, which reflect underlying structural regularities in the input ensemble. In this study, we explored the outcome of this acquisition mechanism, and to this end, we investigated the neural correlates of artificial syntactic classification using event-related functional magnetic resonance imaging. The participants engaged once a day during an 8-day period in a short-term memory acquisition task in which consonant-strings generated from an artificial grammar were presented in a sequential fashion without performance feedback. They performed reliably above chance on the grammaticality classification tasks on days 1 and 8 which correlated with a corticostriatal processing network, including frontal, cingulate, inferior parietal, and middle occipital/occipitotemporal regions as well as the caudate nucleus. Part of the left inferior frontal region (BA 45) was specifically related to syntactic violations and showed no sensitivity to local substring familiarity. In addition, the head of the caudate nucleus correlated positively with syntactic correctness on day 8 but not day 1, suggesting that this region contributes to an increase in cognitive processing fluency.

Adult↗

Effective neural response function for collective population states.

Collective behaviour of neural networks often divides the ensemble of neurons into sub-classes by neuron type; by selective synaptic potentiation; or by mode of stimulation. When the number of classes becomes larger than two, the analysis, even in a mean-field theory, loses its intuitive aspect because of the number of dimensions of the space of dynamical variables. Often one is interested in the behaviour of a reduced set of sub-populations (in focus) and in their dependence on the system's parameters, as in searching for coexistence of spontaneous activity and working memory; in the competition between different working memories; in the competition between working memory and a new stimulus; or in the interaction between selective activity in two different neural modules. For such cases we present a method for reducing the dimensionality of the system to one or two dimensions, even when the total number of populations involved is higher. In the reduced system the familiar intuitive tools apply and the analysis of the dependence of different network states on ambient parameters becomes transparent. Moreover, when the coding of states in focus is sparse, the computational complexity is much reduced. Beyond the analysis, we present a set of detailed examples. We conclude with a discussion of questions of stability in the reduced system.

Animals↗

Cell-assembly coding in several memory processes.

The present paper discusses why the cell assembly, i.e., an ensemble population of neurons with flexible functional connections, is a tenable view of the basic code for information processes in the brain. The main properties indicating the reality of cell-assembly coding are neurons overlaps among different assemblies and connection dynamics within and among the assemblies. The former can be detected as multiple functions of individual neurons in processing different kinds of information. Individual neurons appear to be involved in multiple information processes. The latter can be detected as changes of functional synaptic connections in processing different kinds of information. Correlations of activity among some of the recorded neurons appear to change in multiple information processes. Recent experiments have compared several different memory processes (tasks) and detected these two main properties, indicating cell-assembly coding of memory in the working brain. The first experiment compared different types of processing of identical stimuli, i.e., working memory and reference memory of auditory stimuli. The second experiment compared identical processes of different types of stimuli, i.e., discriminations of simple auditory, simple visual, and configural auditory-visual stimuli. The third experiment compared identical processes of different types of stimuli with or without temporal processing of stimuli, i.e., discriminations of elemental auditory, configural auditory-visual, and sequential auditory-visual stimuli. Some possible features of the cell-assembly coding, especially "dual coding" by individual neurons and cell assemblies, are discussed for future experimental approaches.

Animals↗

Spatiotemporal analysis of prepyriform, visual, auditory, and somesthetic surface EEGs in trained rabbits.

1. Spatial ensemble averages were computed for 64 traces of electroencephalograms (EEGs) simultaneously recorded from 8 x 8 arrays over the epidural surfaces of the prepyriform cortex (PPC) and visual, somatic, and auditory cortices. They revealed a common waveform across each array. Examination of the spatial amplitude modulation (AM) of the waveform revealed classifiable spatial pattern in short time segments. The AM patterns varied within trials after presentation of identical conditioned stimuli, and also between trials with differing stimuli. 2. PPC EEGs revealed strong correlates with the respiratory rhythm; neocortical EEGs did not. 3. Time ensemble averaging of the PPC EEG attenuated the oscillatory bursts, indicating that olfactory gamma oscillations (20-80 Hz) were not phase-locked to the times of stimulus delivery but instead to inhalations. Time ensemble averages of neocortical recordings across trials revealed average evoked potentials starting 30-50 ms after the arrival of the stimulus. 4. Average temporal fast Fourier transform (FFT) power spectral densities (PSDs) from pre- and poststimulus PPC EEG segments revealed a peak of gamma activity in olfactory bursts. 5. The logarithm of the average temporal FFT PSDs from pre- and poststimulus neocortical EEG segments, when plotted against log frequency, revealed 1/f-type spectra in both pre- and poststimulus segments for negative/aversive conditioned stimuli (CS-) and positive/rewarding conditioned stimuli (CS+). The alpha'- and beta'-coefficients from the regression of Eq. 2 onto the average PSDs were significantly different between pre- and poststimulus segments, owing to the evoked potentials, but not between CS- and CS+ stimulus segments. 6. Spatiotemporal patterns were invariant over all frequency bins in the 1/f domain (20-100 Hz). Spatiotemporal patterns in the 2- to 20-Hz domain progressively differed from the invariant patterns with decreasing frequency. 7. In the spatial frequency domain, the logarithm of the average spatial FFT power spectra from pre- and poststimulus neocortical EEG segments, when plotted against the log spatial frequency, fell monotonically from the maximum at the lowest spatial frequency, downwardly curving to a linear 1/f spectral domain. This curve in the 1/f spectral domain extended from 0.133 to 0.880 cycles/mm in the PPC and from 0.095 to 0.624 cycles/mm in the neocortices. 8. Methods of FFT and principal component analysis (PCA) EEG decomposition were used to extract the broad-spectrum waveform common to all 64 EEGs from an array. AM patterns for the FFT and PCA components were derived by regression. They were shown by cross-correlation to yield spatial patterns that were equivalent to each other and to AM patterns from calculation of the 64 root-mean-square amplitudes of the segments. 9. Each spatial AM pattern was expressed by a 1 x 64 column vector and a point in 64-space. Similar patterns formed clusters, and dissimilar patterns gave multiple clusters. A statistical test was devised to evaluate dissimilarity by a Euclidean distance metric in 64-space. 10. Significant spatial pattern classification of CS- versus CS+ trials (below the 1% confidence limit for 20 of each) was found in discrete temporal segments of poststimulus data after digital temporal and spatial filter optimization. 11. Varying the analysis window duration from 10 to 500 ms yielded a window length of 120 ms as optimal for pattern classification. A 120-ms window was subsequently stepped across each record in overlapping intervals of 20 ms. Windows in which episodic, significant CS+/CS- differences occurred lasted 50-200 ms and were separated by 100-200 ms in the poststimulus period. 12. Neocortical spatial patterns changed under reinforcement contingency reversal, showing a lack of invariance in respect to stimuli and a dependence on context and learning, as previously found for the olfactory bulb and PPC.

Animals↗

Neural ensemble coding in inferior temporal cortex.

1. Isolated, single-neuron extracellular potentials were recorded sequentially in area TE of the inferior temporal cortex (IT) of two macaque monkeys (n = 58 and n = 41 neurons). Data were obtained while the animals were performing a paired-associate task. The task utilized five stimuli and eight stimulus pairings (4 correct and 4 incorrect). Data were evaluated as average spike rate during experimental epochs of 100 or 400 ms. Single-unit and population characteristics were measured using a form of linear discriminant analysis and information theoretic measures. To evaluate the significance of covariance on population code measures, additional data consisting of simultaneous recordings from < or = 8 isolated neurons (n = 37) were obtained from a third macaque monkey that was passively viewing visual stimuli. 2. On average, 43% of IT neurons were activated by any of the stimuli used (60% if those inhibited also are included). Yet the neurons were rather unique in the relative magnitude of their responses to each stimulus in the test set. These results suggest that information may be represented in IT by the pattern of activity across neurons and that the representation is not sparsely coded. It is further suggested that the representation scheme may have similarities to DNA or computer codes wherein a coding element is not a local parametric descriptor. This is a departure from the V1 representation, which appears to be both local and parametric. It is also different from theories of IT representation that suggest a constructive basis set or "alphabet". From this view, determination of stimulus discrimination capacity in IT should be evaluated by measures of population activity patterns. 3. Evaluation of small groups of simultaneously recorded neurons obtained during a fixation task suggests that little information about visual stimuli is conveyed by covariance of activity in IT when a 100-ms time scale is used as in this study. This finding is consistent with a prior report, by Gochin et al., which used a 1-ms time scale and failed to find neural activity coherence or oscillations dependent on stimuli. 4. Population-stimulus-discrimination capacity measures were influenced by the number of neurons and to some extent the number and type of stimuli. 5. Information conveyed by individual neurons (mutual information) averaged 0.26 bits. The distribution of information values was unimodal and is therefore more consistent with a distributed than a local coding scheme.(ABSTRACT TRUNCATED AT 400 WORDS)

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