Alessandra Giangrande, Giacinto Luigi Cerone, Alberto Botter, Harri Piitulainen
{"title":"Volitional muscle activation intensifies neuronal processing of proprioceptive afference in the primary sensorimotor cortex: an EEG study.","authors":"Alessandra Giangrande, Giacinto Luigi Cerone, Alberto Botter, Harri Piitulainen","doi":"10.1152/jn.00340.2023","DOIUrl":null,"url":null,"abstract":"<p><p>Proprioception refers to the ability to perceive the position and movement of body segments in space. The cortical aspects of the proprioceptive afference from the body can be investigated using corticokinematic coherence (CKC). CKC accurately quantifies the degree of coupling between cortical activity and limb kinematics, especially if precise proprioceptive stimulation of evoked movements is used. However, there is no evidence on how volitional muscle activation during proprioceptive stimulation affects CKC strength. Twenty-five healthy volunteers (28.8 ± 7 yr, 11 females) participated in the experiment, which included electroencephalographic (EEG), electromyographic (EMG), and kinematic recordings. Ankle-joint rotations (2-Hz) were elicited through a movement actuator in two conditions: <i>passive</i> condition with relaxed ankle and <i>active</i> condition with constant 5-Nm plantar flexion exerted during the stimulation. In total, 6 min of data were recorded per condition. CKC strength was defined as the maximum coherence value among all the EEG channels at the 2-Hz movement frequency for each condition separately. Both conditions resulted in significant CKC peaking at the Cz electrode over the foot area of the primary sensorimotor (SM1) cortex. Stronger CKC was found for the <i>active</i> (0.13 ± 0.14) than the <i>passive</i> (0.03 ± 0.04) condition (<i>P</i> < 0.01). The results indicated that volitional activation of the muscles intensifies the neuronal proprioceptive processing in the SM1 cortex. This finding could be explained both by peripheral sensitization of the ankle joint proprioceptors and central modulation of the neuronal proprioceptive processing at the spinal and cortical levels.<b>NEW & NOTEWORTHY</b> The current study is the first to investigate the effect of volitional muscle activation on CKC-based assessment of cortical proprioception of the ankle joint. Results show that the motor efference intensifies the neuronal processing of proprioceptive afference of the ankle joint. This is a significant finding as it may extend the use of CKC method during active tasks to further evaluate the motor efference-proprioceptive afference relationship and the related adaptations to exercise, rehabilitation, and disease.</p>","PeriodicalId":16563,"journal":{"name":"Journal of neurophysiology","volume":null,"pages":null},"PeriodicalIF":2.1000,"publicationDate":"2024-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of neurophysiology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1152/jn.00340.2023","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2023/11/15 0:00:00","PubModel":"Epub","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Proprioception refers to the ability to perceive the position and movement of body segments in space. The cortical aspects of the proprioceptive afference from the body can be investigated using corticokinematic coherence (CKC). CKC accurately quantifies the degree of coupling between cortical activity and limb kinematics, especially if precise proprioceptive stimulation of evoked movements is used. However, there is no evidence on how volitional muscle activation during proprioceptive stimulation affects CKC strength. Twenty-five healthy volunteers (28.8 ± 7 yr, 11 females) participated in the experiment, which included electroencephalographic (EEG), electromyographic (EMG), and kinematic recordings. Ankle-joint rotations (2-Hz) were elicited through a movement actuator in two conditions: passive condition with relaxed ankle and active condition with constant 5-Nm plantar flexion exerted during the stimulation. In total, 6 min of data were recorded per condition. CKC strength was defined as the maximum coherence value among all the EEG channels at the 2-Hz movement frequency for each condition separately. Both conditions resulted in significant CKC peaking at the Cz electrode over the foot area of the primary sensorimotor (SM1) cortex. Stronger CKC was found for the active (0.13 ± 0.14) than the passive (0.03 ± 0.04) condition (P < 0.01). The results indicated that volitional activation of the muscles intensifies the neuronal proprioceptive processing in the SM1 cortex. This finding could be explained both by peripheral sensitization of the ankle joint proprioceptors and central modulation of the neuronal proprioceptive processing at the spinal and cortical levels.NEW & NOTEWORTHY The current study is the first to investigate the effect of volitional muscle activation on CKC-based assessment of cortical proprioception of the ankle joint. Results show that the motor efference intensifies the neuronal processing of proprioceptive afference of the ankle joint. This is a significant finding as it may extend the use of CKC method during active tasks to further evaluate the motor efference-proprioceptive afference relationship and the related adaptations to exercise, rehabilitation, and disease.
期刊介绍:
The Journal of Neurophysiology publishes original articles on the function of the nervous system. All levels of function are included, from the membrane and cell to systems and behavior. Experimental approaches include molecular neurobiology, cell culture and slice preparations, membrane physiology, developmental neurobiology, functional neuroanatomy, neurochemistry, neuropharmacology, systems electrophysiology, imaging and mapping techniques, and behavioral analysis. Experimental preparations may be invertebrate or vertebrate species, including humans. Theoretical studies are acceptable if they are tied closely to the interpretation of experimental data and elucidate principles of broad interest.