Literature DB >> 27798135

Physiological and Perceptual Sensory Attenuation Have Different Underlying Neurophysiological Correlates.

Clare E Palmer1, Marco Davare2,3, James M Kilner2.   

Abstract

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.
Copyright © 2016 Palmer et al.

Entities:  

Keywords:  electroencephalography; force matching; gamma oscillations; median nerve stimulation; sensory attenuation; somatosensory cortex

Mesh:

Year:  2016        PMID: 27798135      PMCID: PMC5083009          DOI: 10.1523/JNEUROSCI.1694-16.2016

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  36 in total

1.  Central cancellation of self-produced tickle sensation.

Authors:  S J Blakemore; D M Wolpert; C D Frith
Journal:  Nat Neurosci       Date:  1998-11       Impact factor: 24.884

2.  Two eyes for an eye: the neuroscience of force escalation.

Authors:  Sukhwinder S Shergill; Paul M Bays; Chris D Frith; Daniel M Wolpert
Journal:  Science       Date:  2003-07-11       Impact factor: 47.728

3.  Ipsilateral and contralateral SEP components following median nerve stimulation: effects of interfering stimuli applied to the contralateral hand.

Authors:  R Kakigi
Journal:  Electroencephalogr Clin Neurophysiol       Date:  1986-09

4.  Bias in a common EEG and MEG statistical analysis and how to avoid it.

Authors:  J M Kilner
Journal:  Clin Neurophysiol       Date:  2013-04-29       Impact factor: 3.708

5.  Gating of sensory input at spinal and cortical levels during preparation and execution of voluntary movement.

Authors:  Kazuhiko Seki; Eberhard E Fetz
Journal:  J Neurosci       Date:  2012-01-18       Impact factor: 6.167

6.  Attenuation of auditory N1 results from identity-specific action-effect prediction.

Authors:  Gethin Hughes; Andrea Desantis; Florian Waszak
Journal:  Eur J Neurosci       Date:  2013-01-18       Impact factor: 3.386

7.  Influence of concurrent tactile stimulation on somatosensory evoked potentials following posterior tibial nerve stimulation in man.

Authors:  R Kakigi; S J Jones
Journal:  Electroencephalogr Clin Neurophysiol       Date:  1986-03

8.  Action prediction modulates both neurophysiological and psychophysical indices of sensory attenuation.

Authors:  Cedric Roussel; Gethin Hughes; Florian Waszak
Journal:  Front Hum Neurosci       Date:  2014-02-28       Impact factor: 3.169

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Authors:  Harriet Brown; Rick A Adams; Isabel Parees; Mark Edwards; Karl Friston
Journal:  Cogn Process       Date:  2013-06-07

10.  The computational anatomy of psychosis.

Authors:  Rick A Adams; Klaas Enno Stephan; Harriet R Brown; Christopher D Frith; Karl J Friston
Journal:  Front Psychiatry       Date:  2013-05-30       Impact factor: 4.157

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  20 in total

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Review 2.  Tactile suppression in goal-directed movement.

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3.  Nerve-Specific Input Modulation to Spinal Neurons during a Motor Task in the Monkey.

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4.  Gating of Sensory Input at Subcortical and Cortical Levels during Grasping in Humans.

Authors:  Yuming Lei; Recep A Ozdemir; Monica A Perez
Journal:  J Neurosci       Date:  2018-07-05       Impact factor: 6.167

5.  Alpha-band activity in parietofrontal cortex predicts future availability of vibrotactile feedback in prosthesis use.

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6.  Methodological considerations for the force-matching task.

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Journal:  Behav Res Methods       Date:  2022-08-24

7.  Impaired sense of agency and associated confidence in psychosis.

Authors:  Amit Regev Krugwasser; Yonatan Stern; Nathan Faivre; Eiran Vadim Harel; Roy Salomon
Journal:  Schizophrenia (Heidelb)       Date:  2022-04-02

8.  The positive dimension of schizotypy is associated with a reduced attenuation and precision of self-generated touch.

Authors:  Evridiki Asimakidou; Xavier Job; Konstantina Kilteni
Journal:  Schizophrenia (Heidelb)       Date:  2022-06-29

Review 9.  Functional Movement Disorders and Placebo: A Brief Review of the Placebo Effect in Movement Disorders and Ethical Considerations for Placebo Therapy.

Authors:  Bonnie M Kaas; Casey Jo Humbyrd; Alexander Pantelyat
Journal:  Mov Disord Clin Pract       Date:  2018-10-09

10.  Design, Development and Functionality of a Haptic Force-Matching Device for Measuring Sensory Attenuation.

Authors:  David McNaughton; Carlos Bacigalupo; Alicia Georghiades; Alissa Beath; Julia Hush; Michael Jones
Journal:  Behav Res Methods       Date:  2021-05-23
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