Physiological and perceptual sensory attenuation have different underlying neurophysiological correlates
Open accessAbstract
Sensory attenuation, the top-down filtering or gating of afferent information, has been extensively studied in two fields: physiological and perceptual. Physiological sensory attenuation is represented as a decrease in the amplitude of the primary and secondary components of the somatosensory evoked potential (SEP) before and during movement. Perceptual sensory attenuation, described using the analogy of a persons' inability to tickle oneself, is a reduction in the perception of the afferent input of a self-produced tactile sensation due to the central cancellation of the reafferent signal by the efference copy of the motor command to produce the action. The fields investigating these two areas have remained isolated, so the relationship between them is unclear. The current study delivered median nerve stimulation to produce SEPs during a force-matching paradigm (used to quantify perceptual sensory attenuation) in healthy human subjects to determine whether SEP gating correlated with the behavior. Our results revealed that these two forms of attenuation have dissociable neurophysiological correlates and are likely functionally distinct, which has important implications for understanding neurological disorders in which one form of sensory attenuation but not the other is impaired. Time-frequency analyses revealed a negative correlation over sensorimotor cortex between gamma-oscillatory activity and the magnitude of perceptual sensory attenuation. This finding is consistent with the hypothesis that gamma-band power is related to prediction error and that this might underlie perceptual sensory attenuation. SIGNIFICANCE STATEMENT: We demonstrate that there are two functionally and mechanistically distinct forms of sensory gating. The literature regarding somatosensory evoked potential (SEP) gating is commonly cited as a potential mechanism underlying perceptual sensory attenuation; however, the formal relationship between physiological and perceptual sensory attenuation has never been tested. Here, we measured SEP gating and perceptual sensory attenuation in a single paradigm and identified their distinct neurophysiological correlates. Perceptual and physiological sensory attenuation has been shown to be impaired in various patient groups, so understanding the differential roles of these phenomena and how they are modulated in a diseased state is very important for aiding our understanding of neurological disorders such as schizophrenia, functional movement disorders, and Parkinson's disease.
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Physiological sensory attenuation is critical for movement initiation in active inference.
“The first to consider is ‘physiological sensory attenuation’ (Palmer et al. 2016), which is critical for movement initiation in active inference (Brown et al. 2013).”
From Consciousness in active inference: Deep self-models, other minds, and the challenge of psychedelic-induced ego-dissolution (2021) · cites this paper as Palmer et al. 2016
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- Authors
- Palmer, C. E., Davare, M., & Kilner, J. M.
- Affiliations
- UCL Queen Square Institute of Neurology (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2016-10-19
- Volume
- 36
- Issue
- 42
- Pages
- 10803-10812
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5083009
- OpenAlex
- W2534943943
- Cited by
- 96
- References
- 37
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 12 · 2023: 15 · 2022: 13 · 2021: 10 · 2020: 8 · 2019: 7 · 2018: 4 · 2017: 5 · 2016: 1
- FWCI
- 3.61
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Brunel University Research Archive (BURA) (Brunel University London) (submittedVersion)
- Funders
- Wellcome Trust
- Royal Society
- University College London
- Fonds Wetenschappelijk Onderzoek
- Vlaamse regering
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council (BB/J014184/1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Free Will and Agency
- Keywords
- sensory attenuation, somatosensory evoked potentials, gamma oscillations, efference copy, prediction error, sensorimotor cortex, force matching, tickle, neurological disorders
- MeSH terms
- Adult, Afferent Pathways, Electric Stimulation, Electroencephalography, Evoked Potentials, Somatosensory, Female, Humans, Male, Median Nerve, Middle Aged, Movement, Perception, Psychomotor Performance, Sensory Gating, Touch Perception, Young Adult, Healthy Volunteers, Gamma Rhythm, Sensorimotor Cortex
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