Differential contribution of sensorimotor cortex and subthalamic nucleus to unimanual and bimanual hand movements

Abstract:

Why does unilateral deep brain stimulation improve motor function bilaterally? To address this clinical observation, we collected parallel neural recordings from sensorimotor cortex (SMC) and the subthalamic nucleus (STN) during repetitive ipsilateral, contralateral, and bilateral hand movements in patients with Parkinson’s disease. We used a cross-validated electrode-wise encoding model to map electromyography data to the neural signals. Electrodes in the STN encoded movement at a comparable level for both hands, whereas SMC electrodes displayed a strong contralateral bias. To examine representational overlap across the two hands, we trained the model with data from one condition (contralateral hand) and used the trained weights to predict neural activity for movements produced with the other hand (ipsilateral hand). Overall, between-hand generalization was poor, and this limitation was evident in both regions. A similar method was used to probe representational overlap across different task contexts (unimanual vs. bimanual). Task context was more important for the STN compared to the SMC indicating that neural activity in the STN showed greater divergence between the unimanual and bimanual conditions. These results indicate that SMC activity is strongly lateralized and relatively context-free, whereas the STN integrates contextual information with the ongoing behavior.

Authors:

• Christina M. Merrick

• Owen N. Doyle

• Natali E. Gallegos

• Zachary T. Irwin

• Joseph W. Olson

• Christopher L. Gonzalez

• Robert T. Knight

• Richard B. Ivry

• Harrison C. Walker

Date: 2023

DOI: https://doi.org/10.1093/cercor/bhad492

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Deep brain stimulation of the ventrointermediate nucleus of the thalamus to treat essential tremor improves motor sequence learning

Abstract:

The network of brain structures engaged in motor sequence learning comprises the same structures as those involved in tremor, including basal ganglia, cerebellum, thalamus, and motor cortex. Deep brain stimulation (DBS) of the ventrointermediate nucleus of the thalamus (VIM) reduces tremor, but the effects on motor sequence learning are unknown. We investigated whether VIM stimulation has an impact on motor sequence learning and hypothesized that stimulation effects depend on the laterality of electrode location. Twenty patients (age: 38–81 years; 12 female) withVIM electrodes implanted to treat essential tremor (ET) successfully performed a serial reaction time task, varying whether the stimuli followed a repeating pattern or were selected at random, during which VIM-DBS was either on or off. Analyses of variance were applied to evaluate motor sequence learning performance according to reaction times (RTs) and accuracy. An interaction was observed between whether the sequence was repeated or random and whether VIM-DBS was on or off (F[1,18]=7.89,p=.012). Motor sequence learning, reflected by reduced RTs for repeated sequences, was greater with DBS on than off (T[19]=2.34,p=.031). Stimulation location correlated with the degree of motor learning, with greater motor learning when stimulation targeted the lateral VIM (n=23,ρ=0.46;p=.027).These results demonstrate the beneficial effects of VIM-DBS on motor sequence learning in ET patients, particularly with lateral VIM electrode location, and provide evidence for a role for the VIM in motor sequence learning.

Authors:

• Laila Terzic

• Angela Voegtle

• Amr Farahat

• Nanna Hartong

• Imke Galazky

• Slawomir J. Nasuto

• Adriano de Oliveira Andrade

• Robert T. Knight

• Richard B. Ivry

• Jürgen Voges

• Lars Buentjen

• Catherine M. Sweeney-Reed

Date: 2022

DOI: 10.1002/hbm.25989

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Left hemisphere dominance for bilateral kinematic encoding in the human brain

Abstract:

Neurophysiological studies in humans and nonhuman primates have revealed movement representations in both the contralateral and ipsilateral hemispheres. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

authors:

• Christina M Merrick

• Tanner C Dixon

• Assaf Breska

• Jack Lin

• Edward F Chang

• David King-Stephens

• Kenneth D Laxer

• Peter B Weber

• Jose Carmena

• Robert Thomas Knight

• Richard B Ivry

Date: 2022

DOI: : https://doi.org/10.7554/eLife.69977

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Detecting violations of sensory expectancies following cerebellar degeneration: a mismatch negativity study

Authors:

• Torgeir Moberget

• Christina M. Karns

• Leon Y. Deouell

• Magnus Lindgren

• Robert T. Knight

• Richard B. Ivry

Date: 2008

DOI: 10.1016/j.neuropsychologia.2008.03.016

PubMed: 18486157

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Abstract:

Two hypotheses concerning cerebellar function and predictive behavior are the sensory prediction hypothesis and the timing hypothesis. The former postulates that the cerebellum is critical in generating expectancies regarding forthcoming sensory information. The latter postulates that this structure is critical in generating expectancies that are precisely timed; for example, the expected duration of an event or the time between events. As such, the timing hypothesis constitutes a more specific form of prediction. The present experiment contrasted these two hypotheses by examining the mismatch negativity (MMN) response in patients with cerebellar cortical atrophy and matched controls. While watching a silent movie, a stream of task-irrelevant sounds was presented. A standard sound was presented 60% of the time, whereas the remaining sounds deviated from the standard on one of four dimensions: duration, intensity, pitch, or location. The timing between stimuli was either periodic or aperiodic. Based on the sensory prediction hypothesis, the MMN for the patients should be abnormal across all four dimensions. In contrast, the timing hypothesis would predict a selective impairment of the duration MMN. Moreover, the timing hypothesis would also predict that the enhancement of the MMN observed in controls when the stimuli are presented periodically should be attenuated in the patients. Compared to controls, the patients exhibited a delayed latency in the MMN to duration deviants and a similar trend for the intensity deviants, while pitch and location MMNs did not differ between groups. Periodicity had limited and somewhat inconsistent effects. The present results are at odds with a general role for the cerebellum in sensory prediction and provide partial support for the timing hypothesis.

Electrophysiological methods and trans-cranial magnetic stimulation in behavioral neurology and neuropsychology

Authors:

• Leon Y. Deouell

• Richard B. Ivry

• Robert T. Knight

Date: 2003

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