Face Repetition Probability Does Not Affect Repetition Suppression in Macaque Inferotemporal Cortex
Open accessAbstract
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. SIGNIFICANCE STATEMENT 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.
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Vinken et al. failed to observe any evidence of an effect of repetition probability on RS in single-unit or multiunit activity in macaque ML, even when repetitions were task-relevant and repetition probability affected behavior.
“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 of repetition probability on RS in single‐unit or multiunit activity, even when the repetitions were task‐relevant and repetition probability was found to affect the monkeys'”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [72]
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Evaluating the neurophysiological evidence for predictive processing as a model of perception
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- Authors
- Vinken, K., Op de Beeck, H. P., & Vogels, R.
- Affiliations
- KU Leuven (BE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-07-20
- Volume
- 38
- Issue
- 34
- Pages
- 7492-7504
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6596142
- OpenAlex
- W2883872623
- Cited by
- 49
- References
- 71
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 8 · 2023: 4 · 2022: 5 · 2021: 8 · 2020: 10 · 2019: 7 · 2018: 1
- FWCI
- 3.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Lirias (KU Leuven) (submittedVersion, other-oa)
- Funders
- Fonds Wetenschappelijk Onderzoek (G058212N, G.00007.12-Odysseus, G.00007.12, G088916N)
- KU Leuven (PDM/17/186)
- Vlaamse regering (G.00007.12, G088916N)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- repetition suppression, inferior temporal cortex, face processing, predictive coding, perceptual expectations, top-down modulation, local field potentials, gamma oscillations, single-unit activity, macaque, attention
- MeSH terms
- Action Potentials, Adaptation, Physiological, Animals, Brain Mapping, Face, Female, Fixation, Ocular, Macaca mulatta, Magnetic Resonance Imaging, Male, Probability, Temporal Lobe, Visual Perception, Patch-Clamp Techniques, Anticipation, Psychological
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