Face Repetition Probability Does Not Affect Repetition Suppression in Macaque Inferotemporal Cortex

Abstract

Repetition suppression, which refers to reduced neural activity for repeated stimuli, is typically explained by bottom-up or local adaptation mechanisms. However, recent theories have emphasized the role of top-down processes, suggesting that this response reduction reflects the fulfillment of perceptual expectations. To support this, an influential human fMRI study showed that the magnitude of suppression is modulated by the probability of a repetition. No such repetition probability effect was found in macaque inferior temporal (IT) cortex for spiking activity despite the presence of repetition suppression. Contrary to the human fMRI studies that showed an effect of repetition probability, the macaque single-unit study used a large variety of unfamiliar stimuli and the monkeys were not required to attend the stimuli. Here, as in the human fMRI studies, we used faces as stimuli and made the monkeys attend to the stimulus content. We simultaneously recorded spiking activity and local field potentials (LFPs) in the middle lateral face patch (ML) of one monkey (male) and a face-responsive region of another (female). Although we observed significant repetition suppression of spiking activity and high gamma-band LFPs in both animals, there were no effects of repetition probability even when repetitions were task relevant and repetition probability affected behavioral decisions. In conclusion, despite the use of face stimuli and a stimulus-related task, no neural signature of repetition probability was present for faces in a face responsive patch of macaque IT. This further challenges a general perceptual expectation account of repetition suppression. Repetition suppression is a reduced brain activity for repeated stimuli commonly observed across species. In the predictive coding framework, such suppression is thought to reflect fulfilled perceptual expectations. Although this hypothesis is supported by several human fMRI studies reporting an effect of repetition probability on repetition suppression, this could not be replicated in single-cell recordings in monkey inferior temporal (IT) cortex. Subsequent studies narrowed down the conditions for the effect to requiring attention and being limited to particular stimulus categories such as faces. Here, we show that, even under these conditions, repetition suppression in monkey IT neurons is still unaffected by repetition probability, even in a task with a behavioral effect, challenging the perceptual expectation account of repetition suppression.

Evaluating the neurophysiological evidence for predictive processing as a model of perception

“…measured activity in FFA. To address these issues, Vinken et al 72 . recorded neural activity in response to face stimuli in the middle lateral face patch (ML), a macaque homolog of FFA.…”

“…60 Third, Kaliukhovich and Vogels recorded from IT, while Summerfield et al measured activity in FFA. To address these issues, Vinken et al 72 recorded neural activity in response to face stimuli in the middle lateral face patch (ML), a macaque homolog of FFA. Once again, they failed to observe any evidence of an effect 245 Ann.…”

Incorporating neuronal fatigue in deep neural networks captures dynamics of adaptation in neurophysiology and perception

“…This framework stresses the role of top-down modulations by internally generated perceptual expectations rather than neural fatigue. However, repetition suppression can be dissociated in time from expectation effects (Todorovic and de Lange, 2012) and is not modulated by perceptual expectations induced by repetition probability in macaque IT neurons (Kaliukhovich and Vogels, 2014;Vinken et al, 2018). Therefore, we argue that basic repetition suppression does not rely on top-down circuitry and can be explained by feedforward effects of intrinsic neural mechanisms.…”

Diverse temporal dynamics of repetition suppression revealed by intracranial recordings in human ventral temporal cortex

“…Second, subjects participated in an orthogonal fixation task, which did not require top-down attention on the face images. Third, reported effects of stimulus predictability on the magnitude of RS are inconsistent across studies, stimuli, and measurements (Kaliukhovich DA and R Vogels 2011;Kovacs G et al 2013;Tang MF et al 2018;Vinken K et al 2018). Thus, while the prediction error account for RS is an appealing hypothesis, it does explain the presence of RS during our long-lagged paradigm.…”