scholarly journals Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior

Author(s):  
Matthew G. Perich ◽  
Sara Conti ◽  
Marion Badi ◽  
Andrew Bogaard ◽  
Beatrice Barra ◽  
...  

ABSTRACTBehavior relies on continuous influx of sensory information about the body and the environment. In primates, cortex integrates somatic feedback to accurately reach and manipulate objects. Yet, in many experimental regimes motor cortex seems paradoxically to operate as a feedforward, rather than feedback-driven, system. Here, we recorded simultaneously from motor and somatosensory cortex as monkeys performed a naturalistic reaching and object interaction behavior. We studied how unexpected feedback from behavioral errors influences cortical dynamics. Motor cortex generally exhibited robust feedforward dynamics, yet displayed feedback-driven dynamics surrounding correction of behavioral errors. We then decomposed motor cortical activity into orthogonal subspaces capturing communication with somatosensory cortex or behavior-generating dynamics. During error correction, the communication subspace became feedback-driven, while the behavioral subspace maintained feedforward dynamics. We therefore demonstrate that cortical activity is compartmentalized within distinct subspaces that shape the population dynamics, enabling flexible integration of salient inputs with ongoing activity for robust behavior.

2017 ◽  
Vol 7 (1) ◽  
Author(s):  
John E. Downey ◽  
Lucas Brane ◽  
Robert A. Gaunt ◽  
Elizabeth C. Tyler-Kabara ◽  
Michael L. Boninger ◽  
...  

2019 ◽  
Vol 122 (4) ◽  
pp. 1397-1405 ◽  
Author(s):  
Hiroki Ohashi ◽  
Paul L. Gribble ◽  
David J. Ostry

Motor learning is associated with plasticity in both motor and somatosensory cortex. It is known from animal studies that tetanic stimulation to each of these areas individually induces long-term potentiation in its counterpart. In this context it is possible that changes in motor cortex contribute to somatosensory change and that changes in somatosensory cortex are involved in changes in motor areas of the brain. It is also possible that learning-related plasticity occurs in these areas independently. To better understand the relative contribution to human motor learning of motor cortical and somatosensory plasticity, we assessed the time course of changes in primary somatosensory and motor cortex excitability during motor skill learning. Learning was assessed using a force production task in which a target force profile varied from one trial to the next. The excitability of primary somatosensory cortex was measured using somatosensory evoked potentials in response to median nerve stimulation. The excitability of primary motor cortex was measured using motor evoked potentials elicited by single-pulse transcranial magnetic stimulation. These two measures were interleaved with blocks of motor learning trials. We found that the earliest changes in cortical excitability during learning occurred in somatosensory cortical responses, and these changes preceded changes in motor cortical excitability. Changes in somatosensory evoked potentials were correlated with behavioral measures of learning. Changes in motor evoked potentials were not. These findings indicate that plasticity in somatosensory cortex occurs as a part of the earliest stages of motor learning, before changes in motor cortex are observed. NEW & NOTEWORTHY We tracked somatosensory and motor cortical excitability during motor skill acquisition. Changes in both motor cortical and somatosensory excitability were observed during learning; however, the earliest changes were in somatosensory cortex, not motor cortex. Moreover, the earliest changes in somatosensory cortical excitability predict the extent of subsequent learning; those in motor cortex do not. This is consistent with the idea that plasticity in somatosensory cortex coincides with the earliest stages of human motor learning.


2018 ◽  
Author(s):  
Ke Chen ◽  
Roberto Vincis ◽  
Alfredo Fontanini

ABSTRACTDysfunction of motor cortices is thought to contribute to motor disorders such as Parkinson’s disease (PD). However, little is known on the link between cortical dopaminergic loss, abnormalities in motor cortex neural activity and motor deficits. We address the role of dopamine in modulating motor cortical activity by focusing on the anterior lateral motor cortex (ALM) of mice performing a cued-licking task. We first demonstrate licking deficits and concurrent alterations of spiking activity in ALM of mice with unilateral depletion of dopaminergic neurons (i.e., mice injected with 6-OHDA into the medial forebrain bundle). Hemi-lesioned mice displayed delayed licking initiation, shorter duration of licking bouts, and lateral deviation of tongue protrusions. In parallel with these motor deficits, we observed a reduction in the prevalence of cue responsive neurons and altered preparatory activity. Acute and local blockade of D1 receptors in ALM recapitulated some of the key behavioral and neural deficits observed in hemi-lesioned mice. Altogether, our data show a direct relationship between cortical D1 receptor modulation, cue-evoked and preparatory activity in ALM, and licking initiation.SIGNIFICANCE STATEMENTThe link between dopaminergic signaling, motor cortical activity and motor deficits is not fully understood. This manuscript describes alterations in neural activity of the anterior lateral motor cortex (ALM) that correlate with licking deficits in mice with unilateral dopamine depletion or with intra-ALM infusion of dopamine antagonist. The findings emphasize the importance of cortical dopaminergic modulation in motor initiation. These results will appeal not only to researchers interested in cortical control of licking, but also to a broader audience interested in motor control and dopaminergic modulation in physiological and pathological conditions. Specifically, our data suggest that dopamine deficiency in motor cortex could play a role in the pathogenesis of the motor symptoms of Parkinson’s disease.


2021 ◽  
Author(s):  
Ravi Pancholi ◽  
Lauren Ryan ◽  
Simon P Peron

Primary sensory cortex is a key locus of plasticity during learning. Exposure to novel stimuli often alters cortical activity, but isolating cortex-specific dynamics is challenging due to extensive pre-cortical processing. Here, we employ optical microstimulation of pyramidal neurons in layer (L) 2/3 of mouse primary vibrissal somatosensory cortex (vS1) to study cortical dynamics as mice learn to discriminate microstimulation intensity. Tracking activity over weeks using two-photon calcium imaging, we observe a rapid sparsification of the photoresponsive population, with the most responsive neurons exhibiting the largest declines in responsiveness. Following sparsification, the photoresponsive population attains a stable rate of neuronal turnover. At the same time, the photoresponsive population increasingly overlaps with populations encoding whisker movement and touch. Finally, we find that mice with larger declines in responsiveness learn the task more slowly than mice with smaller declines. Our results reveal that microstimulation-evoked cortical activity undergoes extensive reorganization during task learning and that the dynamics of this reorganization impact perception.


2000 ◽  
Vol 78 (11) ◽  
pp. 923-933 ◽  
Author(s):  
Stephen H Scott

Reaching movements to spatial targets require motor patterns at the shoulder to be coordinated carefully with those at the elbow to smoothly move the hand through space. While the motor cortex is involved in this volitional task, considerable debate remains about how this cortical region participates in planning and controlling movement. This article reviews two opposing interpretations of motor cortical function during multi-joint movements. On the one hand, studies performed predominantly on single-joint movement generally support the notion that motor cortical activity is intimately involved in generating motor patterns at a given joint. In contrast, studies on reaching demonstrate correlations between motor cortical activity and features of movement related to the hand, suggesting that the motor cortex may be involved in more global features of the task. Although this latter paradigm involves a multi-joint motor task in which neural activity is correlated with features of movement related to the hand, this neural activity is also correlated to other movement variables. Therefore it is difficult to assess if and how the motor cortex contributes to the coordination of motor patterns at different joints. In particular, present paradigms cannot assess whether motor cortical activity contributes to the control of one joint or multiple joints during whole-arm tasks. The final point discussed in this article is the development of a new experimental device (KINARM) that can both monitor and manipulate the mechanics of the shoulder and elbow independently during multi-joint motor tasks. It is hoped that this new device will provide a new approach for examining how the motor cortex is involved in motor coordination.Key words: reaching movements, biomechanics, motor coordination, proximal arm.


1981 ◽  
Vol 59 (7) ◽  
pp. 748-756 ◽  
Author(s):  
Y. Lamarre ◽  
G. Spidalieri ◽  
J. P. Lund

This article describes the behavior of motor cortex neurons recorded in macaque monkeys (Macaca mulatta) which had been trained to make extension and flexion movements about the elbow in response to auditory, visual, or somesthetic cues. The pattern of activity of 65% of those movement-related neurons which were recorded during both flexion and extension was reciprocally related to the direction of movement. However, the movements of extension and flexion were made by co-contraction of the biceps and triceps in a pattern that did not match that of the motor cortex neurons. The majority of motor cortex neurons had firing frequencies that were related to movement parameters but by their nature could not be directly involved in the control of α motoneurons in both directions of movement. We suggest that they could, instead, control the fusimotor system. It is more likely that α motoneurons are controlled by the 35% of motor cortex neurons that, like the muscles, do not show reciprocal patterns of activity for movements in opposite directions.


Function ◽  
2020 ◽  
Vol 1 (1) ◽  
Author(s):  
Angeliki Vavladeli ◽  
Tanya Daigle ◽  
Hongkui Zeng ◽  
Sylvain Crochet ◽  
Carl C H Petersen

Abstract The brain processes sensory information in a context- and learning-dependent manner for adaptive behavior. Through reward-based learning, relevant sensory stimuli can become linked to execution of specific actions associated with positive outcomes. The neuronal circuits involved in such goal-directed sensory-to-motor transformations remain to be precisely determined. Studying simple learned sensorimotor transformations in head-restrained mice offers the opportunity for detailed measurements of cellular activity during task performance. Here, we trained mice to lick a reward spout in response to a whisker deflection and an auditory tone. Through two-photon calcium imaging of retrogradely labeled neurons, we found that neurons located in primary whisker somatosensory barrel cortex projecting to secondary whisker somatosensory cortex had larger calcium signals than neighboring neurons projecting to primary whisker motor cortex in response to whisker deflection and auditory stimulation, as well as before spontaneous licking. Longitudinal imaging of the same neurons revealed that these projection-specific responses were relatively stable across 3 days. In addition, the activity of neurons projecting to secondary whisker somatosensory cortex was more highly correlated than for neurons projecting to primary whisker motor cortex. The large and correlated activity of neurons projecting to secondary whisker somatosensory cortex might enhance the pathway-specific signaling of important sensory information contributing to task execution. Our data support the hypothesis that communication between primary and secondary somatosensory cortex might be an early critical step in whisker sensory perception. More generally, our data suggest the importance of investigating projection-specific neuronal activity in distinct populations of intermingled excitatory neocortical neurons during task performance.


2018 ◽  
Author(s):  
Britton Sauerbrei ◽  
Jian-Zhong Guo ◽  
Matteo Mischiati ◽  
Wendy Guo ◽  
Mayank Kabra ◽  
...  

AbstractSkillful control of movement is central to our ability to sense and manipulate the world. A large body of work in nonhuman primates has demonstrated that motor cortex provides flexible, time-varying activity patterns that control the arm during reaching and grasping. Previous studies have suggested that these patterns are generated by strong local recurrent dynamics operating autonomously from inputs during movement execution. An alternative possibility is that motor cortex requires coordination with upstream brain regions throughout the entire movement in order to yield these patterns. Here, we developed an experimental preparation in the mouse to directly test these possibilities using optogenetics and electrophysiology during a skilled reach-to-grab-to-eat task. To validate this preparation, we first established that a specific, time-varying pattern of motor cortical activity was required to produce coordinated movement. Next, in order to disentangle the contribution of local recurrent motor cortical dynamics from external input, we optogenetically held the recurrent contribution constant, then observed how motor cortical activity recovered following the end of this perturbation. Both the neural responses and hand trajectory varied from trial to trial, and this variability reflected variability in external inputs. To directly probe the role of these inputs, we used optogenetics to perturb activity in the thalamus. Thalamic perturbation at the start of the trial prevented movement initiation, and perturbation at any stage of the movement prevented progression of the hand to the target; this demonstrates that input is required throughout the movement. By comparing motor cortical activity with and without thalamic perturbation, we were able to estimate the effects of external inputs on motor cortical population activity. Thus, unlike pattern-generating circuits that are local and autonomous, such as those in the spinal cord that generate left-right alternation during locomotion, the pattern generator for reaching and grasping is distributed across multiple, strongly-interacting brain regions.


Author(s):  
Rachel C. Yuan ◽  
Sarah W. Bottjer

ABSTRACTA region within songbird cortex, AId (dorsal intermediate arcopallium), is functionally analogous to motor cortex in mammals and has been implicated in vocal learning during development. AId thus serves as a powerful model for investigating motor cortical contributions to developmental skill learning. We made extracellular recordings in AId of freely behaving juvenile zebra finches and evaluated neural activity during diverse motor behaviors throughout entire recording sessions, including song production as well as hopping, pecking, preening, fluff-ups, beak interactions with cage objects, scratching, and stretching. A large population of single neurons showed significant modulation of activity during singing relative to quiescence. In addition, AId neurons demonstrated heterogeneous response patterns that were evoked during multiple movements, with single neurons often demonstrating excitation during one movement type and suppression during another. Lesions of AId do not disrupt vocal motor output or impair generic movements, suggesting that the responses observed during active behavior do not reflect direct motor drive. Consistent with this idea, we found that some AId neurons showed differential activity during pecking movements depending on the context in which pecks occurred, suggesting that AId circuitry encodes diverse inputs beyond generic motor parameters. Moreover, we found evidence of neurons that did not respond during discrete movements but were nonetheless modulated during active behavioral states compared to quiescence. Taken together, our results support the idea that AId neurons are involved in sensorimotor integration of external sensory inputs and/or internal feedback cues to help modulate goal-directed behaviors.SIGNIFICANCE STATEMENTMotor cortex across taxa receives highly integrated, multi-modal information and has been implicated in both execution and acquisition of complex motor skills, yet studies of motor cortex typically employ restricted behavioral paradigms that target select movement parameters, preventing wider assessment of the diverse sensorimotor factors that can affect motor cortical activity. Recording in AId of freely behaving juvenile songbirds that are actively engaged in sensorimotor learning offers unique advantages for elucidating the functional role of motor cortical neurons. The results demonstrate that a diverse array of factors modulate motor cortical activity and lay important groundwork for future investigations of how multi-modal information is integrated in motor cortical regions to contribute to learning and execution of complex motor skills.


Physiology ◽  
1999 ◽  
Vol 14 (2) ◽  
pp. 64-68
Author(s):  
Apostolos P. Georgopoulos

Motor cortical activity relates to static motor parameters (isometric force, limb position) under static conditions but predominantly to dynamic parameters (change of force, limb velocity) under dynamic conditions. This dual relation conceptually unifies the role of motor cortex in the control of isometric force and movement.


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