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Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions.

ABSTRACT: A challenge for neuroscience is to understand the conscious and unconscious processes underlying construction of willed actions. We investigated the neural substrate of human motor awareness during awake brain surgery. In a first experiment, awake patients performed a voluntary hand motor task and verbally monitored their real-time performance, while different brain areas were transiently impaired by direct electrical stimulation (DES). In a second experiment, awake patients retrospectively reported their motor performance after DES. Based on anatomo-clinical evidence from motor awareness disorders following brain damage, the premotor cortex (PMC) was selected as a target area and the primary somatosensory cortex (S1) as a control area. In both experiments, DES on both PMC and S1 interrupted movement execution, but only DES on PMC dramatically altered the patients' motor awareness, making them unconscious of the motor arrest. These findings endorse PMC as a crucial hub in the anatomo-functional network of human motor awareness.

SUBMITTER: Fornia L

PROVIDER: S-EPMC7000749 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions.

Fornia Luca L Puglisi Guglielmo G Leonetti Antonella A Bello Lorenzo L Berti Anna A Cerri Gabriella G Garbarini Francesca F

Nature communications 20200204 1

A challenge for neuroscience is to understand the conscious and unconscious processes underlying construction of willed actions. We investigated the neural substrate of human motor awareness during awake brain surgery. In a first experiment, awake patients performed a voluntary hand motor task and verbally monitored their real-time performance, while different brain areas were transiently impaired by direct electrical stimulation (DES). In a second experiment, awake patients retrospectively repo ...[more]

PMID: 32019940

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Project description:Rat auditory cortex was subjected to 0.1 mA anodal direct current in seven 10-min sessions on alternate days. Based on the well-known auditory cortex control of olivocochlear regulation through corticofugal projections, auditory brainstem responses (ABRs) were recorded as an indirect test of the effectiveness and reversibility of the multisession protocol of epidural stimulation. Increases of 20-30 dB ABR auditory thresholds shown after epidural stimulation reverted back to control levels 10 min after a single session. However, increases in thresholds revert 4 days after multisession stimulation. Less changes in wave amplitudes and threshold shifts were shown in ABR recorded contralaterally to the electrically stimulated side of the brain. To assess tissue effects of epidural electric stimulation on the brain cortex, well characterized functional anatomical markers of glial cells (GFAP/astrocytes and Iba1/microglial cells) and neurons (c-Fos) were analyzed in alternate serial sections by quantitative immunocytochemistry. Restricted astroglial and microglial reactivity was observed within the cytoarchitectural limits of the auditory cortex. However, interstitial GFAP overstaining was also observed in the ventricular surface and around blood vessels, thus supporting a potential global electrolytic stimulation of the brain. These results correlate with extensive changes in the distribution of c-Fos immunoreactive neurons among layers along sensory cortices after multisession stimulation. Quantitative immunocytochemical analysis supported this idea by showing a significant increase in the number of positive neurons in supragranular layers and a decrease in layer 6 with no quantitative changes detected in layer 5. Our data indicate that epidural stimulation of the auditory cortex induces a reversible decrease in hearing sensitivity due to local, restricted epidural stimulation. A global plastic response of the sensory cortices, also reported here, may be related to electrolytic effects of electric currents.

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Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions.

Publications

Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions.

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