Neural ensemble coding in inferior temporal cortex

Abstract

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)