scholarly journals Motor planning modulates neural activity patterns in early human auditory cortex

2019 ◽  
Author(s):  
Daniel J. Gale ◽  
Corson N. Areshenkoff ◽  
Claire Honda ◽  
Ingrid S. Johnsrude ◽  
J. Randall Flanagan ◽  
...  

AbstractIt is well established that movement planning recruits motor-related cortical brain areas in preparation for the forthcoming action. Given that an integral component to the control of action is the processing of sensory information throughout movement, we predicted that movement planning might also modulate early sensory cortical areas, readying them for sensory processing during the unfolding action. To test this hypothesis, we performed two human functional MRI studies involving separate delayed movement tasks and focused on pre-movement neural activity in early auditory cortex, given its direct connections to the motor system and evidence that it is modulated by motor cortex during movement in rodents. We show that effector-specific information (i.e., movements of the left vs. right hand in Experiment 1, and movements of the hand vs. eye in Experiment 2) can be decoded, well before movement, from neural activity in early auditory cortex. We find that this motor-related information is represented in a separate subregion of auditory cortex than sensory-related information and is present even when movements are cued visually instead of auditorily. These findings suggest that action planning, in addition to preparing the motor system for movement, involves selectively modulating primary sensory areas based on the intended action.

2019 ◽  
Vol 29 (11) ◽  
pp. 4662-4678 ◽  
Author(s):  
Jason P Gallivan ◽  
Craig S Chapman ◽  
Daniel J Gale ◽  
J Randall Flanagan ◽  
Jody C Culham

Abstract The primate visual system contains myriad feedback projections from higher- to lower-order cortical areas, an architecture that has been implicated in the top-down modulation of early visual areas during working memory and attention. Here we tested the hypothesis that these feedback projections also modulate early visual cortical activity during the planning of visually guided actions. We show, across three separate human functional magnetic resonance imaging (fMRI) studies involving object-directed movements, that information related to the motor effector to be used (i.e., limb, eye) and action goal to be performed (i.e., grasp, reach) can be selectively decoded—prior to movement—from the retinotopic representation of the target object(s) in early visual cortex. We also find that during the planning of sequential actions involving objects in two different spatial locations, that motor-related information can be decoded from both locations in retinotopic cortex. Together, these findings indicate that movement planning selectively modulates early visual cortical activity patterns in an effector-specific, target-centric, and task-dependent manner. These findings offer a neural account of how motor-relevant target features are enhanced during action planning and suggest a possible role for early visual cortex in instituting a sensorimotor estimate of the visual consequences of movement.


eLife ◽  
2022 ◽  
Vol 11 ◽  
Author(s):  
Giacomo Ariani ◽  
J Andrew Pruszynski ◽  
Jörn Diedrichsen

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here we used 7T functional magnetic resonance imaging (fMRI) and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.


2005 ◽  
Vol 93 (1) ◽  
pp. 210-222 ◽  
Author(s):  
Michael P. Harms ◽  
John J. Guinan ◽  
Irina S. Sigalovsky ◽  
Jennifer R. Melcher

Functional magnetic resonance imaging (fMRI) of human auditory cortex has demonstrated a striking range of temporal waveshapes in responses to sound. Prolonged (30 s) low-rate (2/s) noise burst trains elicit “sustained” responses, whereas high-rate (35/s) trains elicit “phasic” responses with peaks just after train onset and offset. As a step toward understanding the significance of these responses for auditory processing, the present fMRI study sought to resolve exactly which features of sound determine cortical response waveshape. The results indicate that sound temporal envelope characteristics, but not sound level or bandwidth, strongly influence response waveshapes, and thus the underlying time patterns of neural activity. The results show that sensitivity to sound temporal envelope holds in both primary and nonprimary cortical areas, but nonprimary areas show more pronounced phasic responses for some types of stimuli (higher-rate trains, continuous noise), indicating more prominent neural activity at sound onset and offset. It has been hypothesized that the neural activity underlying the onset and offset peaks reflects the beginning and end of auditory perceptual events. The present data support this idea because sound temporal envelope, the sound characteristic that most strongly influences whether fMRI responses are phasic, also strongly influences whether successive stimuli (e.g., the bursts of a train) are perceptually grouped into a single auditory event. Thus fMRI waveshape may provide a window onto neural activity patterns that reflect the segmentation of our auditory environment into distinct, meaningful events.


2016 ◽  
Vol 116 (6) ◽  
pp. 2857-2868 ◽  
Author(s):  
Jean-Jacques Orban de Xivry ◽  
Philippe Lefèvre

Movement planning consists of choosing the intended endpoint of the movement and selecting the motor program that will bring the effector on the endpoint. It is widely accepted that movement endpoint is updated on a trial-by-trial basis with respect to the observed errors and that the motor program for a given movement follows the rules of optimal feedback control. In this article, we show clear limitations of these theories. First, participants in the current study could not tune their motor program appropriately for each individual trial. This was true even when the participants selected the width of the target that they reached toward or when they had learned the appropriate motor program previously. These data are compatible with the existence of a switching cost for motor planning, which relates to the drop in performance due to an imposed switch of motor programs. This cost of switching shares many features of costs reported in cognitive task switching experiments and, when tested in the same participants, was correlated with it. Second, we found that randomly changing the width of a target over the course of a reaching experiment prevents the motor system from updating the endpoint of movements on the basis of the performance on the previous trial if the width of the target has changed. These results provide new insights into the process of motor planning and how it relates to optimal control theory and to an action selection based on the reward consequences of the motor program rather than that based on the observed error.


2016 ◽  
Author(s):  
Bjöern Brembs

AbstractIn contrast to the long-held assumption that the organization of behavior is best characterized as the perception of a sensory stimulus followed by appropriate response (i.e., “sensorimotor hypothesis”), recent converging evidence from multiple systems and fields of study instead suggests that both ancestral and extant general brain function is best described in operant terms. Rather than specifyng precise behaviors, sensory information - if at all present - interacts with ongoing neural activity to instruct the organism which type of spontaneous, exploratory behavior to generate. Evaluating the ensuing reafferent feedback modifies the nervous system such that ongoing neural activity patterns become biased towards activity that has generated increased appetitive and decreased aversive feedback in the past. The neurobiological mechanisms underlying both the exploratory, spontaneous behaviors as well as those underlying the modifications caused by the feedback are becoming increasingly understood, even on a molecular level. It is straightforward to hypothesize that the constant interaction between ongoing neural activity and the incoming sensory stream allows the organism to balance behavioral flexibility with efficiency to accomplish adaptive behavioral choice in an often unpredictably changing environment.


2020 ◽  
Author(s):  
Giacomo Ariani ◽  
J. Andrew Pruszynski ◽  
Jörn Diedrichsen

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here we used 7T functional magnetic resonance imaging (fMRI) and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger movements. Surprisingly, these activity patterns were similarly strong to those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during movement execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger movement, while activity in S1 and M1 is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.


2018 ◽  
Author(s):  
Eva Berlot ◽  
George Prichard ◽  
Jill O’Reilly ◽  
Naveed Ejaz ◽  
Jörn Diedrichsen

AbstractHand and finger movements are mostly controlled through crossed corticospinal projections from the contralateral hemisphere. During unimanual movements, activity in the contralateral hemisphere is increased while the ipsilateral hemisphere is suppressed below resting baseline. Despite this suppression, unimanual movements can be decoded from ipsilateral activity alone. This indicates that ipsilateral activity patterns represent parameters of ongoing movement, but the origin and functional relevance of these representations is unclear. Here, we asked whether human ipsilateral representations are caused by active movement, or whether they are driven by sensory input. Participants alternated between performing single finger presses and having fingers passively stimulated, while we recorded brain activity using high-field (7T) functional imaging. We contrasted active and passive finger representations in sensorimotor areas of ipsilateral and contralateral hemispheres. Finger representations in the contralateral hemisphere were equally strong under passive and active conditions, highlighting the importance of sensory information in feedback control. In contrast, ipsilateral finger representations were stronger during active presses. Furthermore, the spatial distribution of finger representations differed between hemispheres: the contralateral hemisphere showed the strongest finger representations in Brodmann area 3a and 3b, while the ipsilateral hemisphere exhibited stronger representations in premotor and parietal areas. This suggests that finger representations in the two hemispheres have different origins – contralateral representations are driven by both active movement and sensory stimulation, whereas ipsilateral representations are mainly engaged during active movement. This suggests that a possible contribution of the ipsilateral hemisphere lies in movement planning, rather than in the dexterous feedback control of the movement.Significance statementMovements of the human body are mostly controlled by contralateral cortical regions. However, activity in ipsilateral sensorimotor regions is also modulated during active movements. The origin and functional relevance of these ipsilateral representations is unclear. Here we used high-field neuroimaging to investigate how human contralateral and ipsilateral hemispheres represent active finger presses and passive finger stimulation. We report that while the contralateral hemisphere was equally strongly recruited during active and passive conditions, the ipsilateral hemisphere was mostly recruited during active movement. We propose that the ipsilateral hemisphere may play a role in bilateral movement planning.


2017 ◽  
Author(s):  
Uday K. Jagadisan ◽  
Neeraj J. Gandhi

AbstractThe motor system prepares for movements well in advance of their execution. In the gaze control system, premotor neurons that produce a burst of activity for the movement are also active leading up to the saccade. The dynamics of preparatory neural activity have been well described by stochastic accumulator models, and variability in the accumulation dynamics has been shown to be correlated with reaction times of the eventual saccade, but it is unclear whether this activity is purely preparatory in nature or has features indicative of a hidden movement command. We explicitly tested whether preparatory neural activity in premotor neurons of the primate superior colliculus has “motor potential”. We removed inhibition on the saccadic system using reflex blinks, which turn off downstream gating, and found that saccades can be initiated before underlying activity reaches levels seen under normal conditions. Accumulating low-frequency activity was predictive of eye movement dynamics tens of milliseconds in advance of the actual saccade, indicating the presence of a latent movement command. We also show that reaching threshold is not a necessary condition for movement initiation, contrary to the postulates of accumulation-to-threshold models. The results bring into question extant models of saccade generation and support the possibility of a concurrent representation for movement preparation and generation.Significance StatementHow the brain plans for upcoming actions before deciding to initiate them is a central question in neuroscience. Popular theories suggest that movement planning and execution occur in serial stages, separated by a decision boundary in neural activity space (e.g., “threshold”), which needs to be crossed before the movement is executed. By removing inhibitory gating on the motor system, we show here that the activity required to initiate a saccade can be flexibly modulated. We also show that evolving activity during movement planning is a hidden motor command. The results have important implications for our understanding of how movements are generated, in addition to providing useful information for decoding movement intention based on planning-related activity.Impact StatementNon-invasive disinhibition of the oculomotor system shows that ongoing preparatory activity in the superior colliculus has movement-generating potential and need not rise to threshold in order to produce a saccade.


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