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Scholl, L. R.

Publications and source records attributed to Scholl, L. R..

7 recordsLinked to original sources

Changes to task relevance in redundant motor environments distinguish structure learning from adaptation

Motor actions often exceed the dimensionality of task feedback, which creates control redundancy that requires learners to identify which movement dimensions influence task outcomes. The computations that shape learning in redundant tasks, especially when task-relevant spaces change, remain unclear. We studied this by combining established visuomotor perturbation approaches with a redundant motor interface reaching task. Two monkeys learned a 3D hand position to 2D cursor position mapping that allowed us to define and manipulate the task-relevant space. After animals learned an initial task-relevant space, we introduced two types of perturbations: Relevance Preserving (RP), which rotated hand-cursor relationships within the learned task relevant space, and Relevance Altering (RA), which altered the task relevant space. We hypothesized that RP perturbations would engage error-based adaptation (observed in non-redundant tasks), whereas RA perturbations would engage additional learning mechanisms associated with acquiring new skills. RP perturbations were learned rapidly during training (online) and generalized to the initial learned mapping, consistent with error-based adaptation. In contrast, adapting to the first RA perturbation took longer, engaged learning outside of training (offline), and did not generalize to the initial learned mapping. Animals also adapted faster across repeated exposures to new RA mappings and changed how they generated movements to learn each new mapping, consistent with computations associated with structure learning. These findings suggest that changing task relevance shifts motor learning from adaptation toward structure learning, which has implications for models of motor learning and sensorimotor therapies like brain-computer interfaces.

neuroscience↗

Combining phase analysis and causal stimulation enables longitudinal mesoscale connectivity mapping

Uncovering the circuit mechanisms of flexible behavior requires characterizing how neural signals propagate across large-scale networks and tracking how those networks evolve over time. Signal propagation through networks can be characterized by injecting activity and analyzing signals propagation, thereby measuring "causal connectivity". However, current techniques cannot measure causal connectivity at centimeter scales over weeklong periods of time, especially in non-human primates. Here, we present a stimulation and recording method to longitudinally measure causal connectivity across centimeter-scale cortical networks in macaques. We combined multi-site optogenetic stimulation with micro-electrocorticography using a semi-chronic implant approach that enables stable daily measurements over weeks-long periods spanning years. Stimulation evoked activity reflected a mixture of local, stimulation-driven responses and secondary, delayed activity presumably driven through connections. We applied phase-based spectral analysis to disentangle stimulation-driven and secondary activity related to causal connections. We validated this approach by tracking connectivity across weeks. We demonstrated improved stability over long durations while preserving sensitivity to eyes-open vs. closed behavioral states. This platform provides a robust means to investigate the large-scale circuit dynamics underlying complex behavior in the primate brain.

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The spatiotemporal structure of neural activity in motor cortex during reaching

Intracortical brain-computer interfaces (BCI) leverage knowledge about neural representations to translate movement-related neural activity into actions. BCI implants have targeted broad cortical regions known to have relevant motor representations, but emerging technologies will allow flexible targeting to specific neural populations. The structure of motor representations in neural populations across frontal motor cortices, which span centimeters, has not been well characterized. Here, we investigate how motor representations and population dynamics (temporal coordination) vary across a large expanse of frontal motor cortices. We used high-density, laminar, microelectrode arrays to record many neurons and then sampled neural populations across frontal motor cortex in two monkeys while they performed a reaching task. Our experiments allowed us to map neuronal activity across three spatial dimensions and relate them to movement. Target decoding analysis revealed that target direction information (one key aspect of task information) was heterogeneously distributed across the cortical surface and in depth. Similarly, we found that the temporal dynamics of different neural populations was highly variable, but that the amount of task information predicted which neural populations had similar dynamics. The neural populations with the most similar dynamics were composed of neurons with high task information regardless of spatial location. Our results highlight the spatiotemporal complexity of motor representations across frontal motor cortex at the level of neurons and neural populations, where well-learned movements consistently recruit a spatially distributed subset of neurons. Further insights into the spatiotemporal structure of neural activity patterns across frontal motor cortex will be critical to guide future implants for improved BCI performance. Significance StatementMotor brain-computer interfaces (BCI) translate neural activity into movement, but how to target implants within motor cortices to maximize performance remains unclear. We used high-density recordings of neural activity spanning a large cortical area and related them to movement to map the spatial distribution of task information and the evolution of neural population activity over time. Our measurements revealed that neurons with the most task information were highly distributed across cortex yet also evolved coherently in time, suggesting that spatially distributed neurons coordinate to control movements. Our results provide new links between neuron- and population-level maps of motor representations, and highlight the complex spatiotemporal structure of activity that may need to be considered when designing next-generation BCIs.

neuroscience↗

Mapping eye, arm, and reward information in frontal motor cortices using electrocorticography in non-human primates

Goal-directed reaches give rise to dynamic neural activity across the brain as we move our eyes and arms, and process outcomes. High spatiotemporal resolution mapping of multiple cortical areas will improve our understanding of how these neural computations are spatially and temporally distributed across the brain. In this study, we used micro-electrocorticography ({micro}ECoG) recordings in two male monkeys performing visually guided reaches to map information related to eye movements, arm movements, and receiving rewards over a 1.37 cm2 area of frontal motor cortices (primary motor cortex, premotor cortex, frontal eye field, and dorsolateral pre-frontal cortex). Time-frequency and decoding analyses revealed that eye and arm movement information shifts across brain regions during a reach, likely reflecting shifts from planning to execution. We then used phase-based analyses to reveal potential overlaps of eye and arm information. We found that arm movement decoding performance was impacted by task-irrelevant eye movements, consistent with the presence of intermixed eye and arm information across much of motor cortices. Phase-based analyses also identified reward-related activity primarily around the principal sulcus in the pre-frontal cortex as well as near the arcuate sulcus in the premotor cortex. Our results demonstrate {micro}ECoGs strengths for functional mapping and provide further detail on the spatial distribution of eye, arm, and reward information processing distributed across frontal cortices during reaching. These insights advance our understanding of the overlapping neural computations underlying coordinated movements and reveal opportunities to leverage these signals to enhance future brain-computer interfaces. Significance statement Picking up your coffee mug requires coordinating movements of your eyes and hand and processing the outcomes of those movements. Mapping how neural activity relates to different functions helps us understand how the brain performs these computations. Many mapping techniques have limited spatial or temporal resolution, restricting our ability to dissect computations that overlap closely in space and time. We used micro-electrocorticography recordings to map neural activity across multiple cortical areas while monkeys made goal-directed reaches. These measurements revealed high spatial and temporal resolution maps of neural activity related to eye, arm, and reward information processing. These maps reveal overlapping neural computations underlying movement and open opportunities to use eye and reward information to improve therapies to restore motor function.

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Novel rabies virus variant for bi-directional optical control reveals modulatory influence of the pulvinar on visual cortex in rat

Optogenetic tools have become of great utility in the causal analysis of systems in the brain. However, current optogenetic techniques do not reliably support both excitation and suppression of the same cells in vivo, limiting analysis and slowing research. Here we developed a novel glycoprotein-deleted rabies virus expressing two channelrhodopsin proteins, GtACR2 and Chrimson, in order to independently manipulate excitatory and inhibitory transmembrane potentials, respectively. Using this approach, we demonstrated that rodent pulvinar neurons modulate cortical size tuning and suppress flash responses, but do not drive activity in visual cortex. While our goal was primarily to develop this novel method to study the structure-function organization of thalamocortical circuits, this technique is readily applicable to study any brain region.

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Projections between visual cortex and pulvinar nucleus in the rat

The extrageniculate visual pathway, which carries visual information from the retina through the superficial layers of the superior colliculus and the pulvinar nucleus, is poorly understood. The pulvinar is thought to modulate information flow between cortical areas, and has been implicated in cognitive tasks like directing visually guided actions. In order to better understand the underlying circuitry, we performed retrograde injections of modified rabies virus in the visual cortex and pulvinar of the Long-Evans rat. We found a relatively small population of cells projecting to primary visual cortex (V1), compared to a much larger population projecting to higher visual cortex. Reciprocal corticothalamic projections showed a similar result, implying that pulvinar does not play as big a role in directly modulating V1 activity as previously thought.

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Visual response characteristics in lateral and medial subdivisions of the rat pulvinar

The pulvinar is a higher-order thalamic relay and a central component of the extrageniculate visual pathway, with input from the superior colliculus and visual cortex and output to all of visual cortex. Rodent pulvinar, more commonly called the lateral posterior nucleus (LP), consists of three highly-conserved subdivisions, and offers the advantage of simplicity in its study compared to more subdivided primate pulvinar. Little is known about receptive field properties of LP, let alone whether functional differences exist between different LP subdivisions, making it difficult to understand what visual information is relayed and what kinds of computations the pulvinar might support. Here, we characterized single-cell response properties in two V1 recipient subdivisions of rat pulvinar, the rostromedial (LPrm) and lateral (LPl), and found that a fourth of the cells were selective for orientation, compared to half in V1, and that LP tuning widths were significantly broader. Response latencies were also significantly longer and preferred size more than three times larger on average than in V1; the latter suggesting pulvinar as a source of spatial context to V1. Between subdivisons, LPl cells preferred higher temporal frequencies, whereas LPrm showed a greater degree of direction selectivity and pattern motion detection. Taken together with known differences in connectivity patterns, these results suggest two separate visual feature processing channels in the pulvinar, one in LPl related to higher speed processing which likely derives from superior colliculus input, and the other in LPrm for motion processing derived through input from visual cortex. Significance StatementThe pulvinar has a perplexing role in visual cognition as no clear link has been found between the functional properties of its neurons and behavioral deficits that arise when it is damaged. The pulvinar, called the lateral posterior nucleus (LP) in rats, is a higher order thalamic relay with input from the superior colliculus and visual cortex and output to all of visual cortex. By characterizing single-cell response properties in anatomically distinct subdivisions we found two separate visual feature processing channels in the pulvinar, one in lateral LP related to higher speed processing which likely derives from superior colliculus input, and the other in rostromedial LP for motion processing derived through input from visual cortex.

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