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Prut, Y.

Publications and source records attributed to Prut, Y..

8 recordsLinked to original sources

Deep learning framework for kinematic event detection and stimulation decoding in primate reaching behavior

Accurate analysis of motor behavior requires the reliable detection of ongoing kinematic events and a granular characterization of the changes in motor output that occur in response to neural impairments. This article describes a deep learning framework based on bidirectional long short-term memory (BiLSTM) networks developed to analyze single-trial three-dimensional reaching trajectories recorded from two non-human primates. The framework was used to detect movement onset and corrective turning points, and to differentiate control from the perturbed trials during which cerebellar output was blocked. This approach was compared to manually annotated data. Only small within-animal errors in detecting movement onset times were observed (8.92 {+/-} 2.03 ms and 9.56 {+/-} 3.64 ms for the two monkeys). These errors were significantly smaller (p < 0.001) than those obtained using conventional velocity-threshold methods. Transferring the same detection algorithm from one animal to the other resulted in large errors because the reconstructed workspaces were represented in different coordinate frames. Orthogonal Procrustes alignment substantially reduced the between-animal event-detection errors, and brought performance closer to the within-animal range. Decoding of the perturbed vs. the control trials achieved above-chance levels of accuracy for each animal (accuracies of 71.0% and 61.9% respectively). However, the between-animal generalization was poor (near chance level) and was not improved by geometric alignment. These findings suggest that geometric alignment can support the transfer of shared kinematic event structure between animals, but that perturbation-related changes in movements reflect animal-specific compensatory strategies which cannot be generalized.

animal behavior and cognition↗

Functional organizational principle evaluated by microstimulation in the cortical facial motor areas

Facial gestures are crucial for social interactions among all primates. Since these actions are performed in the absence of direct visual feedback, their effectiveness relies on their stereotypical, almost reflexive patterns. One efficient mechanism for controlling ethological actions could involve motor cortical action maps (Graziano et al., 2002; 2016). Here, we studied whether stereotypical socio-communicative facial expressions are organized into discrete cortical zones by applying long-duration, supra-threshold microstimulation to fMRI-identified cortical areas of the facial motor system. Our findings revealed that these stimulation parameters produced complex facial responses by engaging multiple facial regions but did not elicit social-communicative facial behavior. The effects of long-duration stimulation appeared to be an amplified (both spatially and temporally) version of the responses seen with short-duration stimulation. The stimulation-evoked neural activity extended across the facial motor system, suggesting that these cortical regions function as part of a large-scale network designed to generate coherent, context-specific, and socially relevant motor outputs.

neuroscience↗

Neural Synchrony Links Sensorimotor Cortices in a Network for Facial Motor Control

Primate societies rely on the production and interpretation of social signals, in particular those displayed by the face. Facial movements are controlled, according to the dominant neuropsychological schema, by two separate circuits, one originating in medial frontal cortex controlling emotional expressions, and a second one originating in lateral motor and premotor areas controlling voluntary facial movements. Despite this functional dichotomy, cortical anatomy suggests that medial and lateral areas are directly connected and may thus operate as a single network. Here we test these contrasting hypotheses through structural and functional magnetic resonance imaging (fMRI) guided electrical stimulation and simultaneous multi-channel recordings from key facial motor areas in the macaque monkey brain. These areas include medial facial motor area M3 (located in the anterior cingulate cortex); two lateral face-related motor areas: M1 (primary motor) and PMv (ventrolateral premotor); and S1 (primary somatosensory cortex). Cortical responses evoked by intracortical stimulation revealed that medial and lateral areas can exert significant functional impact on each other. Simultaneous recordings of local field potentials in all facial motor areas further confirm that during facial expressions, medial and lateral facial motor areas significantly interact, primarily in the alpha and beta frequency ranges, whereas during voluntary chewing, coupling occurs at lower frequencies. These functional interactions varied across facial movement types. Thus, at the cortical level, the control of facial movements is not mediated through independent (medial/lateral) functional streams, but results from an interacting sensorimotor network. Significance StatementPrimates communicate through facial expressions. How the brain generates facial expressions remains poorly understood. To uncover how facial motor-related cortical brain regions interact to produce facial gestures, we combined fMRI-targeted electrophysiology and intracortical microstimulation while monkeys produced qualitatively different facial movements. Our two-pronged experimental approach revealed that facial motor-related cortical areas form an interconnected network characterized by synchronized neural activity demonstrating dynamic expression-selective activity states that are coordinated across the network nodes. Thus, the multiple facial motor-related cortical areas sending axons directly into the facial nucleus operate as a single network in which the overall complex, behavior-specific inter-areal interactions dictate the relevant motor output.

neuroscience↗

Cerebellar output shapes cortical preparatory activity during motor adaptation

The cerebellum plays a key role in motor adaptation by driving trial-to-trial recalibration of movements based on previous errors. In primates, cortical correlates of adaptation are encoded already in the pre-movement motor plan, but these early cortical signals could be driven by a cerebellar-to-cortical information flow or evolve independently through intracortical mechanisms. To address this question, we trained female macaque monkeys to reach against a viscous force field (FF) while blocking cerebellar outflow. The cerebellar block led to impaired FF adaptation and a compensatory, re-aiming-like shift in motor cortical preparatory activity. In the null-field conditions, the cerebellar block altered neural preparatory activity by increasing task-representation dimensionality and impeding generalization. A computational model indicated that low-dimensional (cerebellar-like) feedback is sufficient to replicate these findings. We conclude that cerebellar signals carry task structure information that constrains the dimensionality of the cortical preparatory manifold and promotes generalization. In the absence of these signals, cortical mechanisms are harnessed to partially restore adaptation.

neuroscience↗

Disentangling acute motor deficits and adaptive responses evoked by the loss of cerebellar output

Patients with cerebellar damage experience various motor impairments, but the specific sequence of primary and compensatory processes that contribute to these deficits remains unclear. To clarify this, we reversibly blocked cerebellar outflow in monkeys engaged in planar reaching tasks. This intervention led to a spatially selective reduction in hand velocity, primarily due to decreased muscle torque, especially in movements requiring high inter-joint torque coupling. When examining repeated reaches to the same target, we found that the reduced velocity resulted from both an immediate deficit and a gradually developing compensatory slowing to reduce passive inter-joint interactions. However, the slowed hand velocity did not account for the fragmented and variable movement trajectories observed during the cerebellar block. Our findings indicate that cerebellar impairment results in motor deficits due to both inadequate muscle torque and an altered motor control strategy for managing impaired limb dynamics. Additionally, impaired motor control elevates noise, which cannot be entirely mitigated through compensatory strategies.

neuroscience↗

Cortical inhibitory network selects cerebellar signals for movement initiation

The onset of voluntary movements is driven by coordinated firing across a large population of motor cortical neurons. This pattern of activity is determined by both local interactions and long-range corticocortical and subcortical inputs. The way remote areas of the brain communicate to effectively drive movement is still unclear. We addressed this question by studying an important pathway through which the cerebellum communicates, via the motor thalamus, with the motor cortex. We found that similar to the sensory cortices, thalamic input to the motor cortex triggers feedforward inhibition by directly contacting inhibitory cells via particularly effective GluR2- lacking AMPA receptors blocked by NASPM. Based on these results, we constructed a classifier for SCP-responsive cortical cells to identify pyramidal and PV interneurons and study their role in controlling movements. The findings indicate that PV and pyramidal cells are co-driven by TC input in response to activation of the CTC pathway. During task performance, PV and pyramidal cells had comparable relations to movement parameters (directional tuning and movement duration). However, PV interneurons exhibited stronger movement-related activity that preceded the firing of pyramidal cells. This seemingly counterintuitive sequence of events where inhibitory cells are recruited more strongly and before excitatory cells may in fact enhance the signal-to-noise ratio of cerebellar signals by suppressing other inputs and prioritizing the excitatory synchronized volley from the TC system which occurs at the right time to overcome the inhibitory signal. In this manner, the CTC system can shape cortical activity in a way that exceeds its sheer synaptic efficacy.

neuroscience↗

Motor cortical plasticity in response to skill acquisition in adult monkeys

Cortical maps often undergo plastic changes during learning or in response to injury. In sensory areas, these changes are thought to be triggered by alterations in the pattern of converging inputs and a functional reassignment of the deprived cortical region. In the motor cortex, training on a task that engages distal effectors was shown to increase their cortical representation (as measured by response to intracortical microstimulation). However, this expansion could be a specific outcome of using a demanding dexterous task. We addressed this question by measuring the long-term changes in cortical maps of monkeys that were sequentially trained on two different tasks involving either proximal or distal joints. We found that motor cortical remodeling in adult monkeys was symmetric such that both distal and proximal movements can comparably alter motor maps in a fully reversible manner according to task demands. Further, we found that the change in mapping often included a switch between remote joints (e.g., a finger site switched to a shoulder site) and reflected a usage-consistent reorganization of the map rather than the local expansion of one representation into nearby sites. Finally, although cortical maps were considerably affected by the performed task, motor cortical neurons throughout the motor cortex were equally likely to fire in a task-related manner independent of the task and/or the recording site. These results may imply that in the motor system, enhanced motor efficiency is achieved through a dynamical allocation of larger cortical areas and not by specific recruitment of task-relevant cells.

neuroscience↗

Reversible block of cerebellar outflow reveals cortical circuitry for motor coordination

Coordinated movements are achieved by selecting muscles and activating them at specific times. This process relies on intact cerebellar circuitry, as demonstrated by motor impairments triggered by cerebellar lesions. Based on anatomical connectivity and symptoms observed in cerebellar patients, we hypothesized that cerebellar dysfunction should disrupt the temporal patterns of motor cortical activity but not the selected motor plan. To test this hypothesis, we reversibly blocked cerebellar outflow in primates while monitoring motor behavior and neural activity. This manipulation replicated the impaired motor timing and coordination characteristic of cerebellar ataxia. We found extensive changes in motor cortical activity, including a loss of response transients at movement onset and a decoupling of task-related activity. Nonetheless, the spatial tuning of cells was unaffected and their early preparatory activity was mostly intact. These results indicate that the timing of actions, but not the selection of muscles, is regulated through cerebellar control of motor cortical activity.\n\nHIGHLIGHTSO_LIHigh frequency stimulation blocked cerebellar outflow and impaired motor behavior\nC_LIO_LIResponse patterns and coordinated firing of CTC neurons were disrupted\nC_LIO_LIThe spatial tuning and early preparatory activity of neurons were unaffected\nC_LIO_LICerebellar control of local and global cortical synchrony supports motor timing\nC_LI\n\nIN BRIEFNashef et al. used high frequency stimulation to block cerebellar outflow. This manipulation impaired motor timing and coordination similarly to symptoms found in cerebellar patients. In parallel, the response patterns of cortical neurons and cell-to-cell synchronization were altered, yet spatial tuning was maintained. Motor timing and coordination are regulated by a dedicated cerebellar signal that organizes execution-related activity of a motor cortical subnetwork.

neuroscience↗