Recent human functional magnetic resonance imaging studies (Summerfield C, Trittschuh EH, Monti JM, Mesulam MM, Egner T. 2008. Neural repetition suppression reflects fulfilled perceptual expectations. Nat Neurosci. 11:1004-1006.) showed that adaptation or repetition suppression is affected by contextual factors related to perceptual expectations, suggesting that adaptation results from a fulfillment of perceptual expectation or a reduction in prediction error. This view contrasts with the bottom-up fatigue or sharpening mechanisms of adaptation proposed in single-cell studies. We examined whether stimulus repetition probability affects adaptation of spiking activity and local field potentials (LFPs) in macaque inferior temporal (IT) cortex, using a protocol similar to that of Summerfield et al. Monkeys were exposed to 2 randomly interleaved trials, each consisting of either 2 identical (rep trial) or 2 different stimuli (alt trial). Trials were presented in repetition (rep) blocks consisting of 75% of rep trials and 25% of alt trials or in alternation (alt) blocks having opposite repetition probabilities. For both spiking and LFP activities, the stimulus-selective adaptation did not differ significantly between rep and alt blocks. The number of preceding rep or alt trials and the trial position within a block did not affect adaptation. This absence of any effect of stimulus repetition probability on adaptation suggests that adaptation in IT is not caused by contextual factors related to perceptual expectation.

Previously several functional magnetic resonance imaging (fMRI) studies point toward the role of perceptual expectations in determining adaptation or repetition suppression (RS) in humans. These studies showed that the probability of repetitions of faces within a block influences the magnitude of adaptation in face-related areas of the human brain (Summerfield et al., 2008). However, a current macaque single-cell/local field potential (LFP) recording study using objects as stimuli found no evidence for the modulation of the neural response by the repetition probability in the inferior temporal cortex (Kaliukhovich and Vogels, 2010). Here we examined whether stimulus repetition probability affects fMRI repetition suppression for nonface object stimuli in the human brain. Subjects were exposed to either two identical [repetition trials (RTs)] or two different [alternation trials (ATs)] object stimuli. Both types of trials were presented blocks consisting of either 75% [repetition blocks (RBs)] or 25% [alternation blocks (ABs)] of RTs. We found strong RS, i.e., a lower signal for RTs compared to ATs, in the object sensitive lateral occipital cortex as well as in the face-sensitive occipital and fusiform face areas. More importantly, however, there was no significant difference in the magnitude of RS between RBs and ABs in each of the areas. This is in agreement with the previous monkey single-unit/LFP findings and suggests that RS in the case of nonface visual objects is not modulated by the repetition probability in humans. Our results imply that perceptual expectation effects vary for different visual stimulus categories.

Many studies measured neural responses in oddball paradigms, showing a different response to the same stimulus when presented with a low (deviant) compared with a high probability (standard) in a sequence. Such a differential response is manifested in event-related potential studies as the mismatch negativity (MMN) and has been observed in several sensory modalities, including vision. Other studies showed that stimulus repetition suppresses the neural response. It has been suggested that this adaptation effect underlies the smaller responses to the standard compared with the deviant stimulus in oddball sequences. However, the MMN may also reflect the violation of a prediction based on the sequence of standards, i.e., a surprise response. We examined the presence of a surprise response to deviants in visual oddball sequences in macaque (Macaca mulatta) inferior temporal (IT) cortex, a higher-order cortical area. In agreement with visual MMN studies, single-unit IT responses were greater for the deviant than for the standard stimuli. However, single IT neurons showed no greater response to the deviant stimulus in the oddball sequence than to the same stimulus presented with the same probability in a sequence that consisted of many stimuli. LFPs also showed no evidence of a surprise response. These data suggest that stimulus-specific adaptation, without a surprise-related boost of activity to the deviant, underlies the responses in visual oddball sequences even in higher visual cortex. Furthermore, we show that for IT neurons such adaptive mechanisms take into account a relatively short stimulus history, with weaker effects at longer time scales.

Kaliukhovich DA, Vogels R. Stimulus repetition affects both strength and synchrony of macaque inferior temporal cortical activity. J Neurophysiol 107: 3509 -3527, 2012. First published April 4, 2012 doi:10.1152/jn.00059.2012.-Repetition of a visual stimulus reduces the firing rate of macaque inferior temporal (IT) neurons. The neural mechanisms underlying this adaptation or repetition suppression are still unclear. In particular, we do not know how the IT circuit is affected by stimulus repetition. To address this, we measured local field potentials (LFPs) and multiunit spiking activity (MUA) simultaneously at 16 sites with a laminar electrode in IT while repeating visual images. Stimulus exposures and interstimulus intervals were each 500 ms. The rhesus monkeys were performing a passive fixation task during the recordings. Induced LFP power decreased with repetition for spectral frequencies above 60 Hz but increased with repetition for lower frequencies, the latter because of a delayed decrease in power when repeating a stimulus. LFP-LFP and MUA-LFP coherences decreased with repetition for frequencies above 60 Hz. This repetition suppression of the MUA-LFP coherence was not due to differences in firing rate since it was present when spike counts were equated for the adapter and repeated stimuli. For frequencies between 15 and 40 Hz, the effect of repetition on synchronization depended on the electrode depth: For the putative superficial layers synchronization was enhanced with repetition, while the LFPs of the putative deep layers decreased their synchrony across layers. The between-site, trial-to-trial covariations in MUA ("noise correlations") decreased with repetition, but this might have reflected repetition suppression of the firing rate. This work demonstrates that short-term stimulus repetition affects the synchronized activity, in addition to response strength, in IT cortex.inferior temporal cortex; multiunit activity; local field potentials THE RESPONSES of many macaque inferior temporal (IT) neurons decrease with stimulus repetition (Baylis and Rolls 1987;

Stimulus repetition alters neural responses to the repeated stimulus. This so-called adaptation phenomenon has been commonly observed at multiple spatial and temporal scales and in different brain areas, and has been hypothesized to affect the neural representation of the sensory input. Yet, the neural mechanisms underlying adaptation still remain unclear, especially in higher-order cortical areas. Here we employ a divisive normalization model of neural responses to predict adaptation-induced changes in responses of single neurons in the macaque inferior temporal (IT) cortex. According to this model, the response of a neuron is determined by an interplay between its direct excitatory and divisive normalizing inputs, with each input being subject to adaptation. To test the model, we recorded the responses of single IT cortex neurons to complex visual stimuli while separately adapting the two putative types of input to those neurons. We compared the changes in responses of these neurons following such adaptation with predictions derived from the divisive normalization model. As predicted by the model, we show that adaptation in the IT cortex can, depending on the relative strength of each putative type of input to a neuron, suppress or enhance the neural response to a complex stimulus. More generally, our data suggest that adaptation serves to selectively enhance processing of the stimuli that differ from recently experienced ones, even when these occur within a configuration of multiple stimuli.