Elsevier

Cortex

Volume 80, July 2016, Pages 185-195
Cortex

Special issue: Review
Sources of adaptation of inferior temporal cortical responses

https://doi.org/10.1016/j.cortex.2015.08.024Get rights and content

Abstract

Neurons of different brain regions change their response when a stimulus is repeated. In inferior temporal cortex (IT), stimulus repetition typically reduces the responses of single neurons, i.e., IT neurons show repetition suppression. Single unit recordings in IT showed that individual neurons vary in their degree of adaptation effects, ranging from strong suppression to slight enhancement of the response to the repeated stimulus. The suppression is maximal after the peak of the response and then reduces during the further course of the response. Repetition suppression in IT is still present for interstimulus intervals of at least 900 msec. I discuss the contribution of mechanisms that have been proposed to explain adaptation effects of IT responses. Firing-rate dependent response fatigue, e.g., a prolonged hyperpolarization, intrinsic to the recorded neuron cannot explain the stimulus specificity of the adaptation effect. The latter can be explained by synaptic depression or an adapted input from other IT neurons. We observed repetition suppression of IT neurons when adapter and test stimuli were presented at locations that differed by 8 degree of visual angle, suggesting that at least part of the adaptation effect is not inherited from retinotopic visual areas with small receptive fields. We observed no effect of repetition probability on repetition suppression in macaque IT using images of various categories, suggesting a dissociation between top-down expectation effects and repetition suppression. Together, our data agree with the hypothesis that adaptation in IT serves to reduce the saliency of recently seen stimuli, highlighting stimuli that differ from recently presented ones.

Section snippets

Short-term adaptation: paradigm and phenomenology of adaptation effects

In this paper, I will discuss the underlying mechanisms of adaptation in macaque IT, relating these to observations made in single unit recording studies. I will discuss mainly short-term adaptation studies, in which the stimuli are presented for relatively short durations (as in most fMRI-adaptation studies) and without intervening stimuli (unlike in “priming” – related studies). It is well possible that the mechanisms of short-term adaptation differ at least to some extent from those

Response fatigue

The mechanism initially thought to underlie repetition suppression and commonly assumed in accounts of fMRI adaptation is spike frequency-dependent “fatigue” or “response fatigue”: firing spikes will decrease the firing rate of the neuron during subsequent stimulation. Such spiking-dependent suppression has been demonstrated in the primary visual cortex of cats (Sanchez-Vives et al., 2000a, Sanchez-Vives et al., 2000b). In these studies, it was shown that an artificial membrane depolarization

Attention and adaptation effects

Stimulus-specific adaptation may be related to differences in attention between the adapter and test stimuli: a repeated stimulus may be attended less than a “novel” stimulus and this decreased attention corresponds to a suppressed neural response to the repeated stimulus. Note that this can mean that a repeated stimulus engages less bottom-up, exogeneous attention or that a repeated stimulus will engage less top-down, endogenous attention. The former possibility leads to a chicken and egg

Adaptation as a manifestation of a reduced prediction error

A recent alternative model of adaptation stresses the role of top-down factors in generating repetition suppression (Friston, 2005, Summerfield et al., 2008). In that model, repetition suppression is a consequence of the fulfillment of perceptual expectations or of a reduced mismatch between expected and observed percepts, i.e., a reduced prediction error. Thus, repetition suppression should occur when the subject expects that a stimulus will be repeated (low prediction error), and there should

Function of adaptation in IT

Speculating about the function of adaptation and repetition suppression in IT is difficult given our current lack of a precise understanding of the mechanisms underlying adaptation. However, the known phenomenology of adaptation effects in IT and the effect of adaptation on neural representations can be of help in building a hypothesis about the function of adaptation in IT. Adaptation reduces selectively the response to a stimulus that is identical to the one seen recently. Kaliukhovich, De

Acknowledgments

The author would like to thank the contributions of Dr. H. Sawamura, Dr. W. De Baene and Dr. D. Kaliukhovich to the work reviewed here. Also, I would like to thank D. Kaliukhovich, P. Kuravi and K. Vinken for critical reading of a draft of this paper. The work from the author's laboratory was supported by Fonds voor Wetenschappelijk Onderzoek Vlaanderen (G.0582.12N), Interuniversitaire Attractiepool and Programma Financiering (PF 10/008) and the European Community's Seventh Framework Program

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