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Efference Copy Is Necessary for the Attenuation of Self-Generated Touch.

ABSTRACT: Self-generated touch feels less intense than external touch of the same intensity. According to theory, this is because the brain predicts and attenuates the somatosensory consequences of our movements using a copy of the motor command, i.e., the efference copy. However, whether the efference copy is necessary for this somatosensory attenuation is unclear. Alternatively, a predictable contact of two body parts could be sufficient. Here we quantified the attenuation of touch applied on the participants' left index finger when the touch was triggered by the active or passive movement of the right index finger and when it was externally generated. We observed attenuation only when the touch was triggered by the participants' active movement. In contrast, during the passive movement, the touch was perceived to be as strong as when the touch was externally triggered. Our results suggest that the efference copy is necessary for the attenuation of self-generated touch.

SUBMITTER: Kilteni K

PROVIDER: S-EPMC6997587 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Efference Copy Is Necessary for the Attenuation of Self-Generated Touch.

Kilteni Konstantina K Engeler Patrick P Ehrsson H Henrik HH

iScience 20200116 2

Self-generated touch feels less intense than external touch of the same intensity. According to theory, this is because the brain predicts and attenuates the somatosensory consequences of our movements using a copy of the motor command, i.e., the efference copy. However, whether the efference copy is necessary for this somatosensory attenuation is unclear. Alternatively, a predictable contact of two body parts could be sufficient. Here we quantified the attenuation of touch applied on the partic ...[more]

PMID: 32058957

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Project description:Since the early 1970s, numerous behavioral studies have shown that self-generated touch feels less intense and less ticklish than the same touch applied externally. Computational motor control theories have suggested that cerebellar internal models predict the somatosensory consequences of our movements and that these predictions attenuate the perception of the actual touch. Despite this influential theoretical framework, little is known about the neural basis of this predictive attenuation. This is due to the limited number of neuroimaging studies, the presence of conflicting results about the role and the location of cerebellar activity, and the lack of behavioral measures accompanying the neural findings. Here, we combined psychophysics with fMRI to detect the neural processes underlying somatosensory attenuation in male and female healthy human participants. Activity in bilateral secondary somatosensory areas was attenuated when the touch was presented during a self-generated movement (self-generated touch) than in the absence of movement (external touch). An additional attenuation effect was observed in the cerebellum that is ipsilateral to the passive limb receiving the touch. Importantly, we further found that the degree of functional connectivity between the ipsilateral cerebellum and the contralateral primary and bilateral secondary somatosensory areas was linearly and positively related to the degree of behaviorally assessed attenuation; that is, the more participants perceptually attenuated their self-generated touches, the stronger this corticocerebellar coupling. Collectively, these results suggest that the ipsilateral cerebellum is fundamental in predicting self-generated touch and that this structure implements somatosensory attenuation via its functional connectivity with somatosensory areas.SIGNIFICANCE STATEMENT When we touch our hand with the other, the resulting sensation feels less intense than when another person or a machine touches our hand with the same intensity. Early computational motor control theories have proposed that the cerebellum predicts and cancels the sensory consequences of our movements; however, the neural correlates of this cancelation remain unknown. By means of fMRI, we show that the more participants attenuate the perception of their self-generated touch, the stronger the functional connectivity between the cerebellum and the somatosensory cortical areas. This provides conclusive evidence about the role of the cerebellum in predicting the sensory feedback of our movements and in attenuating the associated percepts via its connections to early somatosensory areas.

Project description:BackgroundA 'continuum of psychosis' refers to the concept that psychotic-like experiences occur to certain extents in the healthy population and to more severe extents in individuals with psychotic disorders. If this concept is valid, neurophysiological abnormalities exhibited by patients with schizophrenia should also be present, to some degree, in non-clinical individuals who score highly on the personality dimension of schizotypy. Patients with schizophrenia have consistently been shown to exhibit electrophysiological suppression abnormalities to self-generated speech. The present study aimed to investigate whether these electrophysiological suppression abnormalities were also present in non-clinical individuals who scored highly on schizotypy.MethodsThirty-seven non-clinical individuals scoring High (above median) and 37 individuals scoring Low (below median) on the Schizotypal Personality Questionnaire (SPQ; a commonly used schizotypy scale) underwent electroencephalographic (EEG) recording. The amplitude of the N1 component of the auditory-evoked potential was measured while participants (a) vocalized simple syllables (Talk condition), (b) passively listened to a recording of these vocalizations (Listen condition) and (c) listened to a recording of the vocalizations while simultaneously watching a video depicting the sound-wave of the forthcoming vocalizations, allowing them to be temporally predicted (Cued Listen condition).ResultsThe Low Schizotypy group exhibited significantly reduced N1-amplitude in the Talk condition relative to both the Listen and Cued Listen conditions; that is, they exhibited significant N1-suppression. The High Schizotypy group exhibited significantly lower levels of N1-suppression compared to the Low Schizotypy group. Furthermore, while the Cued Listen condition induced significantly lower N1-amplitudes compared to the Listen condition in the Low Schizotypy group, this was not the case for the High Schizotypy group.ConclusionsThe results suggest that non-clinical, highly schizotypal individuals exhibit subnormal levels of N1-suppression to self-generated speech, similar to the N1-suppression abnormalities which have previously been reported in patients with schizophrenia. This finding provides empirical support for the existence of a neurophysiological 'continuum of psychosis'.

Dataset Information

Efference Copy Is Necessary for the Attenuation of Self-Generated Touch.

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Efference Copy Is Necessary for the Attenuation of Self-Generated Touch.

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