Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback

Christensen, Mark Schram; Lundbye‐Jensen, Jesper; Geertsen, Svend Sparre; Petersen, Tue Hvass; Paulson, Olaf B.; Nielsen, Jens Bo

doi:10.1038/nn1873

Cited by 172 publications

(150 citation statements)

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“…Our findings are in agreement with previous studies that demonstrate enhanced evoked activity to self-generated stimuli in auditory (Reznik et al, 2014), somatosensory (Simões-Franklin et al, 2011;Ackerley et al, 2012), and visual (Hughes and Waszak, 2011) cortices compared with otherwise identical sensory stimuli perceived in a passive manner. These studies suggest that an efference copy enhances the neural response evoked by the sensory consequences of self-generated actions (see also Christensen et al, 2007). Other studies report attenuated responses to self-generated stimuli and suggest a canceling role of an efference copy in sensory cortices (Blakemore et al, 1998;Martikainen et al, 2005;Aliu et al, 2009;Baess et al, 2009;Saupe et al, 2013;Horváth, 2014;Timm et al, 2014).…”

Section: Discussionmentioning

confidence: 91%

“…The magnitude of such modifications in sensory cortices has been previously reported to be mediated by the amount of motor output (Cui et al, 2014), and its source is believed to lie within the motor system, although its exact origin remains unknown. One study points to the ventral pre-motor cortex as a candidate brain region providing efferent signals to somatosensory cortex (Christensen et al, 2007), while other studies point to the cerebellum (Blakemore et al, 1998;Knolle et al, 2012Knolle et al, , 2013). Yet another study suggests the involvement of supplementary motor area (SMA; Haggard and Whitford, 2004).…”

Section: Introductionmentioning

confidence: 99%

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Enhanced Auditory Evoked Activity to Self-Generated Sounds Is Mediated by Primary and Supplementary Motor Cortices

2015

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Accumulating evidence demonstrates that responses in auditory cortex to auditory consequences of self-generated actions are modified relative to the responses evoked by identical sounds generated by an external source. Such modifications have been suggested to occur through a corollary discharge sent from the motor system, although the exact neuroanatomical origin is unknown. Furthermore, since tactile input has also been shown to modify responses in auditory cortex, it is not even clear whether the source of such modifications is motor output or somatosensory feedback. We recorded functional magnetic resonance imaging (fMRI) data from healthy human subjects (n ϭ 11) while manipulating the rate at which they performed sound-producing actions with their right hand. In addition, we manipulated the amount of tactile feedback to examine the relative roles of motor and somatosensory cortices in modifying evoked activity in auditory cortex (superior temporal gyrus). We found an enhanced fMRI signal in left auditory cortex during perception of self-generated sounds relative to passive listening to identical sounds. Moreover, the signal difference between active and passive conditions in left auditory cortex covaried with the rate of sound-producing actions and was invariant to the amount of tactile feedback. Together with functional connectivity analysis, our results suggest motor output from supplementary motor area and left primary motor cortex as the source of signal modification in auditory cortex during perception of self-generated sounds. Motor signals from these regions could represent a predictive signal of the expected auditory consequences of the performed action.

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Section: Discussionmentioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Enhanced Auditory Evoked Activity to Self-Generated Sounds Is Mediated by Primary and Supplementary Motor Cortices

2015

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“…Right ventral premotor cortex is an area that has been shown to modulate primary somatosensory cortex activations (Christensen et al, 2007) and right orbital frontal cortex is thought to represent anticipatory activity related to the expected sensory consequences of sensorimotor tasks (Schoenbaum et al, 2009). The right hemispheric nature of these and other correlated regions in this study aligns well with both our previous proprioceptive mapping work (Goble et al, 2011) and that of colleagues (2005, 2007), who found right hemisphere dominance for muscle spindle feedback processing.…”

Section: Discussionmentioning

confidence: 99%

Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults

Goble¹,

Coxon²,

Impe³

et al. 2011

J. Neurosci.

176

124

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Proprioceptive information from the foot/ankle provides important information regarding body sway for balance control, especially in situations where visual information is degraded or absent. Given known increases in catastrophic injury due to falls with older age, understanding the neural basis of proprioceptive processing for balance control is particularly important for older adults. In the present study, we linked neural activity in response to stimulation of key foot proprioceptors (i.e., muscle spindles) with balance ability across the lifespan. Twenty young and 20 older human adults underwent proprioceptive mapping; foot tendon vibration was compared with vibration of a nearby bone in an fMRI environment to determine regions of the brain that were active in response to muscle spindle stimulation. Several body sway metrics were also calculated for the same participants on an eyes-closed balance task. Based on regression analyses, multiple clusters of voxels were identified showing a significant relationship between muscle spindle stimulation-induced neural activity and maximum center of pressure excursion in the anterior-posterior direction. In this case, increased activation was associated with greater balance performance in parietal, frontal, and insular cortical areas, as well as structures within the basal ganglia. These correlated regions were age-and foot-stimulation side-independent and largely localized to right-sided areas of the brain thought to be involved in monitoring stimulus-driven shifts of attention. These findings support the notion that, beyond fundamental peripheral reflex mechanisms, central processing of proprioceptive signals from the foot is critical for balance control.

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“…Using ischaemic nerve block it has been shown that during voluntary movement, functional magnetic resonance imaging (fMRI) signal in primary somatosensory cortex (S1) is enhanced (even in the lack of sensory feedback) and functional connectivity with pre-motor cortex is increased, suggesting an enhancing effect of a motor efference copy 19 . Similarly, using positron-emission tomography it has been shown that increases in speech production rate result in increased cerebral blood flow in auditory cortices even when auditory feedback was blocked by white noise that was kept constant across rates 20 .…”

mentioning

confidence: 99%

Lateralized enhancement of auditory cortex activity and increased sensitivity to self-generated sounds

et al. 2014

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Performing actions with auditory consequences modulates the response in auditory cortex to otherwise identical stimuli passively heard. Such modulation has been suggested to occur through a corollary discharge sent from the motor cortex during voluntary actions. However, the relationship between the effector used to generate the sound, type of modulation and changes in perceptual sensitivity are unclear. Here we use functional magnetic resonance imaging on healthy subjects and demonstrate bilateral enhancement in the auditory cortex to self-generated versus externally generated sounds. Furthermore, we find that this enhancement is stronger when the sound-producing hand is contralateral to the auditory cortex. At the behavioural level, binaural hearing thresholds are lower for self-generated sounds and monaural thresholds are lower for sounds triggered by the hand ipsilateral to the stimulated ear. Together with functional connectivity analysis, our results suggest that a corollary discharge sent from active motor cortex enhances activity in the auditory cortex and increases perceptual sensitivity in a lateralized manner.

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Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback

Cited by 172 publications

References 13 publications

Enhanced Auditory Evoked Activity to Self-Generated Sounds Is Mediated by Primary and Supplementary Motor Cortices

Enhanced Auditory Evoked Activity to Self-Generated Sounds Is Mediated by Primary and Supplementary Motor Cortices

Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults

Lateralized enhancement of auditory cortex activity and increased sensitivity to self-generated sounds

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