A Mixed Reality Platform for Systematic Investigation of the Neural Mechanisms of Multisensory Integration During Motor Planning

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Description
Multisensory integration is the process by which information from different sensory modalities is integrated by the nervous system. This process is important not only from a basic science perspective but also for translational reasons, e.g., for the development of closed-loo

Multisensory integration is the process by which information from different sensory modalities is integrated by the nervous system. This process is important not only from a basic science perspective but also for translational reasons, e.g., for the development of closed-loop neural prosthetic systems. A mixed virtual reality platform was developed to study the neural mechanisms of multisensory integration for the upper limb during motor planning. The platform allows for selection of different arms and manipulation of the locations of physical and virtual target cues in the environment. The system was tested with two non-human primates (NHP) trained to reach to multiple virtual targets. Arm kinematic data as well as neural spiking data from primary motor (M1) and dorsal premotor cortex (PMd) were collected. The task involved manipulating visual information about initial arm position by rendering the virtual avatar arm in either its actual position (veridical (V) condition) or in a different shifted (e.g., small vs large shifts) position (perturbed (P) condition) prior to movement. Tactile feedback was modulated in blocks by placing or removing the physical start cue on the table (tactile (T), and no-tactile (NT) conditions, respectively). Behaviorally, errors in initial movement direction were larger when the physical start cue was absent. Slightly larger directional errors were found in the P condition compared to the V condition for some movement directions. Both effects were consistent with the idea that erroneous or reduced information about initial hand location led to movement direction-dependent reach planning errors. Neural correlates of these behavioral effects were probed using population decoding techniques. For small shifts in the visual position of the arm, no differences in decoding accuracy between the T and NT conditions were observed in either M1 or PMd. However, for larger visual shifts, decoding accuracy decreased in the NT condition, but only in PMd. Thus, activity in PMd, but not M1, may reflect the uncertainty in reach planning that results when sensory cues regarding initial hand position are erroneous or absent.
Date Created
2023
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Modifying Motor Skill Learning via Neuromodulation of Frontoparietal Networks

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Description
Motor skill learning is important to rehabilitation, sports, and many occupations. When attempting to learn or adapt a motor skill, some individuals learn slower or less compared to others despite the same amount of motor practice. This dissertation aims to

Motor skill learning is important to rehabilitation, sports, and many occupations. When attempting to learn or adapt a motor skill, some individuals learn slower or less compared to others despite the same amount of motor practice. This dissertation aims to understand the factors that contributed to such variability in motor learning, and thereby identify viable methods to enhance motor learning. Behavioral evidence from our lab showed that visuospatial ability is positively related to the extent of motor learning. Neuroimaging studies suggest that motor learning and visuospatial processes share common frontoparietal neural structures, and that this visuospatial-motor relationship may be more pronounced in the right hemisphere compared to the left. Thus, the overall objective of this dissertation is to determine if aspects of motor learning (such as the rate and extent of skill acquisition) may be modifiable through neuromodulation of the right frontoparietal network. In Aim 1, anodal transcranial direct current stimulation (tDCS) was used to test whether modulating the right parietal area affects visuospatial ability and motor skill acquisition. A randomized, three-arm design was used, which added a no-tDCS control group to the double-blinded sham-control protocol to address placebo effects. No tDCS treatment effect was observed, likely due to low statistical power to detect any treatment effects as the study is still ongoing. However, the current results revealed a unique finding that the placebo effect of tDCS was stronger than its treatment effect on motor learning, with implications that tDCS and motor studies should measure and control for placebo effects. In Aim 2, right frontoparietal connectivity during resting-state EEG was estimated via alpha band imaginary coherence to test whether it correlated with visuospatial performance and motor skill acquisition. As a preliminary step towards leveraging the frontoparietal network for EEG-neurofeedback applications, this work found that alpha imaginary coherence was positively correlated with visuospatial function, but not with motor skill acquisition during a limited dose of motor practice (only 5 trials). This work establishes a premise for developing frontoparietal alpha IC-based neurofeedback for cognitive training in rehabilitation, while warranting future studies to test the relationship between alpha IC and motor learning with a more extensive motor training regimen.
Date Created
2021
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Neural mechanisms of sensory integration: frequency domain analysis of spike and field potential activity during arm position maintenance with and without visual feedback

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Description
Understanding where our bodies are in space is imperative for motor control, particularly for actions such as goal-directed reaching. Multisensory integration is crucial for reducing uncertainty in arm position estimates. This dissertation examines time and frequency-domain correlates of

Understanding where our bodies are in space is imperative for motor control, particularly for actions such as goal-directed reaching. Multisensory integration is crucial for reducing uncertainty in arm position estimates. This dissertation examines time and frequency-domain correlates of visual-proprioceptive integration during an arm-position maintenance task. Neural recordings were obtained from two different cortical areas as non-human primates performed a center-out reaching task in a virtual reality environment. Following a reach, animals maintained the end-point position of their arm under unimodal (proprioception only) and bimodal (proprioception and vision) conditions. In both areas, time domain and multi-taper spectral analysis methods were used to quantify changes in the spiking, local field potential (LFP), and spike-field coherence during arm-position maintenance.

In both areas, individual neurons were classified based on the spectrum of their spiking patterns. A large proportion of cells in the SPL that exhibited sensory condition-specific oscillatory spiking in the beta (13-30Hz) frequency band. Cells in the IPL typically had a more diverse mix of oscillatory and refractory spiking patterns during the task in response to changing sensory condition. Contrary to the assumptions made in many modelling studies, none of the cells exhibited Poisson-spiking statistics in SPL or IPL.

Evoked LFPs in both areas exhibited greater effects of target location than visual condition, though the evoked responses in the preferred reach direction were generally suppressed in the bimodal condition relative to the unimodal condition. Significant effects of target location on evoked responses were observed during the movement period of the task well.

In the frequency domain, LFP power in both cortical areas was enhanced in the beta band during the position estimation epoch of the task, indicating that LFP beta oscillations may be important for maintaining the ongoing state. This was particularly evident at the population level, with clear increase in alpha and beta power. Differences in spectral power between conditions also became apparent at the population level, with power during bimodal trials being suppressed relative to unimodal. The spike-field coherence showed confounding results in both the SPL and IPL, with no clear correlation between incidence of beta oscillations and significant beta coherence.
Date Created
2017
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Gamma Band Oscillation Response to Somatosensory Feedback Stimulation Schemes Constructed on Basis of Biphasic Neural Touch Representation

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Description
Prosthetic users abandon devices due to difficulties performing tasks without proper graded or interpretable feedback. The inability to adequately detect and correct error of the device leads to failure and frustration. In advanced prostheses, peripheral nerve stimulation can be

Prosthetic users abandon devices due to difficulties performing tasks without proper graded or interpretable feedback. The inability to adequately detect and correct error of the device leads to failure and frustration. In advanced prostheses, peripheral nerve stimulation can be used to deliver sensations, but standard schemes used in sensorized prosthetic systems induce percepts inconsistent with natural sensations, providing limited benefit. Recent uses of time varying stimulation strategies appear to produce more practical sensations, but without a clear path to pursue improvements. This dissertation examines the use of physiologically based stimulation strategies to elicit sensations that are more readily interpretable. A psychophysical experiment designed to investigate sensitivities to the discrimination of perturbation direction within precision grip suggests that perception is biomechanically referenced: increased sensitivities along the ulnar-radial axis align with potential anisotropic deformation of the finger pad, indicating somatosensation uses internal information rather than environmental. Contact-site and direction dependent deformation of the finger pad activates complimentary fast adapting and slow adapting mechanoreceptors, exhibiting parallel activity of the two associate temporal patterns: static and dynamic. The spectrum of temporal activity seen in somatosensory cortex can be explained by a combined representation of these distinct response dynamics, a phenomenon referred in this dissertation to “biphasic representation.” In a reach-to-precision-grasp task, neurons in somatosensory cortex were found to possess biphasic firing patterns in their responses to texture, orientation, and movement. Sensitivities seem to align with variable deformation and mechanoreceptor activity: movement and smooth texture responses align with potential fast adapting activation, non-movement and coarse texture responses align with potential increased slow adapting activation, and responses to orientation are conceptually consistent with coding of tangential load. Using evidence of biphasic representations’ association with perceptual priorities, gamma band phase locking is used to compare responses to peripheral nerve stimulation patterns and mechanical stimulation. Vibrotactile and punctate mechanical stimuli are used to represent the practical and impractical percepts commonly observed in peripheral nerve stimulation feedback. Standard patterns of constant parameters closely mimic impractical vibrotactile stimulation while biphasic patterns better mimic punctate stimulation and provide a platform to investigate intragrip dynamics representing contextual activation.
Date Created
2017
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Investigating compensatory mechanisms for sound localization: visual cue integration and the precedence effect

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Description
Sound localization can be difficult in a reverberant environment. Fortunately listeners can utilize various perceptual compensatory mechanisms to increase the reliability of sound localization when provided with ambiguous physical evidence. For example, the directional information of echoes can be perceptually

Sound localization can be difficult in a reverberant environment. Fortunately listeners can utilize various perceptual compensatory mechanisms to increase the reliability of sound localization when provided with ambiguous physical evidence. For example, the directional information of echoes can be perceptually suppressed by the direct sound to achieve a single, fused auditory event in a process called the precedence effect (Litovsky et al., 1999). Visual cues also influence sound localization through a phenomenon known as the ventriloquist effect. It is classically demonstrated by a puppeteer who speaks without visible lip movements while moving the mouth of a puppet synchronously with his/her speech (Gelder and Bertelson, 2003). If the ventriloquist is successful, sound will be “captured” by vision and be perceived to be originating at the location of the puppet. This thesis investigates the influence of vision on the spatial localization of audio-visual stimuli. Participants seated in a sound-attenuated room indicated their perceived locations of either ISI or level-difference stimuli in free field conditions. Two types of stereophonic phantom sound sources, created by modulating the inter-stimulus time interval (ISI) or level difference between two loudspeakers, were used as auditory stimuli. The results showed that the light cues influenced auditory spatial perception to a greater extent for the ISI stimuli than the level difference stimuli. A binaural signal analysis further revealed that the greater visual bias for the ISI phantom sound sources was correlated with the increasingly ambiguous binaural cues of the ISI signals. This finding suggests that when sound localization cues are unreliable, perceptual decisions become increasingly biased towards vision for finding a sound source. These results support the cue saliency theory underlying cross-modal bias and extend this theory to include stereophonic phantom sound sources.
Date Created
2015
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The role of motor cortical neuron subpopulations in the adaptation of locomotion through complex environments

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Description
Locomotion in natural environments requires coordinated movements from multiple body parts, and precise adaptations when changes in the environment occur. The contributions of the neurons of the motor cortex underlying these behaviors are poorly understood, and especially little is

Locomotion in natural environments requires coordinated movements from multiple body parts, and precise adaptations when changes in the environment occur. The contributions of the neurons of the motor cortex underlying these behaviors are poorly understood, and especially little is known about how such contributions may differ based on the anatomical and physiological characteristics of neurons. To elucidate the contributions of motor cortical subpopulations to movements, the activity of motor cortical neurons, muscle activity, and kinematics were studied in the cat during a variety of locomotion tasks requiring accurate foot placement, including some tasks involving both expected and unexpected perturbations of the movement environment. The roles of neurons with two types of neuronal characteristics were studied: the existence of somatosensory receptive fields located at the shoulder, elbow, or wrist of the contralateral forelimb; and the existence projections through the pyramidal tract, including fast- and slow-conducting subtypes.

Distinct neuronal adaptations between simple and complex locomotion tasks were observed for neurons with different receptive field properties and fast- and slow-conducting pyramidal tract neurons. Feedforward and feedback-driven kinematic control strategies were observed for adaptations to expected and unexpected perturbations, respectively, during complex locomotion tasks. These kinematic differences were reflected in the response characteristics of motor cortical neurons receptive to somatosensory information from different parts of the forelimb, elucidating roles for the various neuronal populations in accommodating disturbances in the environment during behaviors. The results show that anatomical and physiological characteristics of motor cortical neurons are important for determining if and how neurons are involved in precise control of locomotion during natural behaviors.
Date Created
2015
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Perturbing neural feedback loops to understand the relationships of their parts

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Description
The basal ganglia are four sub-cortical nuclei associated with motor control and reward learning. They are part of numerous larger mostly segregated loops where the basal ganglia receive inputs from specific regions of cortex. Converging on these inputs are dopaminergic

The basal ganglia are four sub-cortical nuclei associated with motor control and reward learning. They are part of numerous larger mostly segregated loops where the basal ganglia receive inputs from specific regions of cortex. Converging on these inputs are dopaminergic neurons that alter their firing based on received and/or predicted rewarding outcomes of a behavior. The basal ganglia's output feeds through the thalamus back to the areas of the cortex where the loop originated. Understanding the dynamic interactions between the various parts of these loops is critical to understanding the basal ganglia's role in motor control and reward based learning. This work developed several experimental techniques that can be applied to further study basal ganglia function. The first technique used micro-volume injections of low concentration muscimol to decrease the firing rates of recorded neurons in a limited area of cortex in rats. Afterwards, an artificial cerebrospinal fluid flush was injected to rapidly eliminate the muscimol's effects. This technique was able to contain the effects of muscimol to approximately a 1 mm radius volume and limited the duration of the drug effect to less than one hour. This technique could be used to temporarily perturb a small portion of the loops involving the basal ganglia and then observe how these effects propagate in other connected regions. The second part applied self-organizing maps (SOM) to find temporal patterns in neural firing rate that are independent of behavior. The distribution of detected patterns frequency on these maps can then be used to determine if changes in neural activity are occurring over time. The final technique focused on the role of the basal ganglia in reward learning. A new conditioning technique was created to increase the occurrence of selected patterns of neural activity without utilizing any external reward or behavior. A pattern of neural activity in the cortex of rats was selected using an SOM. The pattern was then reinforced by being paired with electrical stimulation of the medial forebrain bundle triggering dopamine release in the basal ganglia. Ultimately, this technique proved unsuccessful possibly due to poor selection of the patterns being reinforced.
Date Created
2014
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Investigating spectra of spiking behavior in area 5 of the parietal cortex

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Description
In order to successfully implement a neural prosthetic system, it is necessary to understand the control of limb movements and the representation of body position in the nervous system. As this development process continues, it is becoming increasingly important to

In order to successfully implement a neural prosthetic system, it is necessary to understand the control of limb movements and the representation of body position in the nervous system. As this development process continues, it is becoming increasingly important to understand the way multiple sensory modalities are used in limb representation. In a previous study, Shi et al. (2013) examined the multimodal basis of limb position in the superior parietal lobule (SPL) as monkeys reached to and held their arm at various target locations in a frontal plane. Visual feedback was withheld in half the trials, though non-visual (i.e. somatic) feedback was available in all trials. Previous analysis showed that some of the neurons were tuned to limb position and that some neurons had their response modulated by the presence or absence of visual feedback. This modulation manifested in decreases in firing rate variability in the vision condition as compared to nonvision. The decreases in firing rate variability, as shown through decreases in both the Fano factor of spike counts and the coefficient of variation of the inter-spike intervals, suggested that changes were taking place in both trial-by-trial and intra-trial variability. I sought to further probe the source of the change in intra-trial variability through spectral analysis. It was hypothesized that the presence of temporal structure in the vision condition would account for a regularity in firing that would have decreased intra-trial variability. While no peaks were apparent in the spectra, differences in spectral power between visual conditions were found. These differences are suggestive of unique temporal spiking patterns at the individual neuron level that may be influential at the population level.
Date Created
2013
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The internal representation of arm position revealed through the spatial pattern of hand location estimation errors

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Description
Our ability to estimate the position of our body parts in space, a fundamentally proprioceptive process, is crucial for interacting with the environment and movement control. For proprioception to support these actions, the Central Nervous System has to rely on

Our ability to estimate the position of our body parts in space, a fundamentally proprioceptive process, is crucial for interacting with the environment and movement control. For proprioception to support these actions, the Central Nervous System has to rely on a stored internal representation of the body parts in space. However, relatively little is known about this internal representation of arm position. To this end, I developed a method to map proprioceptive estimates of hand location across a 2-d workspace. In this task, I moved each subject's hand to a target location while the subject's eyes were closed. After returning the hand, subjects opened their eyes to verbally report the location of where their fingertip had been. Then, I reconstructed and analyzed the spatial structure of the pattern of estimation errors. In the first couple of experiments I probed the structure and stability of the pattern of errors by manipulating the hand used and tactile feedback provided when the hand was at each target location. I found that the resulting pattern of errors was systematically stable across conditions for each subject, subject-specific, and not uniform across the workspace. These findings suggest that the observed structure of pattern of errors has been constructed through experience, which has resulted in a systematically stable internal representation of arm location. Moreover, this representation is continuously being calibrated across the workspace. In the next two experiments, I aimed to probe the calibration of this structure. To this end, I used two different perturbation paradigms: 1) a virtual reality visuomotor adaptation to induce a local perturbation, 2) and a standard prism adaptation paradigm to induce a global perturbation. I found that the magnitude of the errors significantly increased to a similar extent after each perturbation. This small effect indicates that proprioception is recalibrated to a similar extent regardless of how the perturbation is introduced, suggesting that sensory and motor changes may be two independent processes arising from the perturbation. Moreover, I propose that the internal representation of arm location might be constructed with a global solution and not capable of local changes.
Date Created
2012
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Influence of sensorimotor noise on the planning and control of reaching in 3-dimensional space

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Description
The ability to plan, execute, and control goal oriented reaching and grasping movements is among the most essential functions of the brain. Yet, these movements are inherently variable; a result of the noise pervading the neural signals underlying sensorimotor processing.

The ability to plan, execute, and control goal oriented reaching and grasping movements is among the most essential functions of the brain. Yet, these movements are inherently variable; a result of the noise pervading the neural signals underlying sensorimotor processing. The specific influences and interactions of these noise processes remain unclear. Thus several studies have been performed to elucidate the role and influence of sensorimotor noise on movement variability. The first study focuses on sensory integration and movement planning across the reaching workspace. An experiment was designed to examine the relative contributions of vision and proprioception to movement planning by measuring the rotation of the initial movement direction induced by a perturbation of the visual feedback prior to movement onset. The results suggest that contribution of vision was relatively consistent across the evaluated workspace depths; however, the influence of vision differed between the vertical and later axes indicate that additional factors beyond vision and proprioception influence movement planning of 3-dimensional movements. If the first study investigated the role of noise in sensorimotor integration, the second and third studies investigate relative influence of sensorimotor noise on reaching performance. Specifically, they evaluate how the characteristics of neural processing that underlie movement planning and execution manifest in movement variability during natural reaching. Subjects performed reaching movements with and without visual feedback throughout the movement and the patterns of endpoint variability were compared across movement directions. The results of these studies suggest a primary role of visual feedback noise in shaping patterns of variability and in determining the relative influence of planning and execution related noise sources. The final work considers a computational approach to characterizing how sensorimotor processes interact to shape movement variability. A model of multi-modal feedback control was developed to simulate the interaction of planning and execution noise on reaching variability. The model predictions suggest that anisotropic properties of feedback noise significantly affect the relative influence of planning and execution noise on patterns of reaching variability.
Date Created
2012
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