Neurons in Macaque Inferior Temporal Cortex Show No Surprise Response to Deviants in Visual Oddball Sequences
Open accessAbstract
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.
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There is conflicting evidence regarding whether IT neurons are sensitive to statistical regularities present in nonadjacent stimuli from a sequence of images or whether these suppression effects are determined by the immediately preceding stimulus.
“There is also conflicting evidence regarding whether IT neurons are sensitive to statistical regularities present in nonadjacent stimuli from a sequence of images 91 or whether these suppression effects are determined by the immediately preceding stimulus. 89 , 96”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [96]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredA number of direct recording studies have produced the opposite pattern to Bell et al., with unexpected or random stimuli eliciting reduced responses relative to expected or neutral stimuli in macaque IT and rodent V1.
“The picture is further complicated by the fact that a number of direct recording studies have produced the opposite pattern of results to Bell et al., with unexpected or random stimuli eliciting reduced responses relative to expected or neutral stimuli in macaque IT 95 , 96 and rodent V1 52 (see Ref. 97 for corresponding results in a human study).”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [96]
Because ES is typically calculated by comparing expected and unexpected stimulus responses, it is often unclear whether it represents genuine suppression, suppression relative to enhanced deviant responses, or both.
“as ES is typically calculated by comparing expected and unexpected stimulus responses, it is often unclear if it represents genuine suppression, suppression relative to the enhanced response to deviant stimuli, or both.”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [96]
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“Particularly telling is how predictive coding advocates responded when single-unit recordings in macaque IT cortex by Kaliukhovich and Vogels (2014) failed to show the expected repetition suppression effects.”
- Authors
- Kaliukhovich, D. A., & Vogels, R.
- Affiliations
- KU Leuven (BE)
- ORCID
- Kaliukhovich, D. A.
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-09-17
- Volume
- 34
- Issue
- 38
- Pages
- 12801-12815
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6705328
- OpenAlex
- W2051537466
- Cited by
- 69
- References
- 70
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 6 · 2023: 3 · 2022: 7 · 2021: 6 · 2020: 6 · 2019: 7 · 2018: 8 · 2017: 6 · 2016: 7 · 2015: 6 · 2014: 1
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Lirias (acceptedVersion, other-oa)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Keywords
- visual oddball, mismatch negativity, inferior temporal cortex, macaque, single-unit responses, local field potentials, stimulus-specific adaptation, prediction violation
- MeSH terms
- Action Potentials, Animals, Evoked Potentials, Visual, Female, Fixation, Ocular, Macaca, Male, Neurons, Photic Stimulation, Temporal Lobe, Visual Perception, Uncertainty
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