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24 Janelia Publications

Showing 1-10 of 24 results
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    07/29/21 | Disrupting cortico-cerebellar communication impairs dexterity.
    Guo J, Sauerbrei BA, Cohen JD, Mischiati M, Graves AR, Pisanello F, Branson KM, Hantman AW
    eLife. 2021 Jul 29;10:. doi: 10.7554/eLife.65906

    To control reaching, the nervous system must generate large changes in muscle activation to drive the limb toward the target, and must also make smaller adjustments for precise and accurate behavior. Motor cortex controls the arm through projections to diverse targets across the central nervous system, but it has been challenging to identify the roles of cortical projections to specific targets. Here, we selectively disrupt cortico-cerebellar communication in the mouse by optogenetically stimulating the pontine nuclei in a cued reaching task. This perturbation did not typically block movement initiation, but degraded the precision, accuracy, duration, or success rate of the movement. Correspondingly, cerebellar and cortical activity during movement were largely preserved, but differences in hand velocity between control and stimulation conditions predicted from neural activity were correlated with observed velocity differences. These results suggest that while the total output of motor cortex drives reaching, the cortico-cerebellar loop makes small adjustments that contribute to the successful execution of this dexterous movement.

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    06/15/21 | A cerebellar-thalamocortical pathway drives behavioral context-dependent movement initiation.
    Dacre J, Colligan M, Clarke T, Ammer JJ, Schiemann J, Chamosa-Pino V, Claudi F, Harston JA, Eleftheriou C, Pakan JM, Huang C, Hantman AW, Rochefort NL, Duguid I
    Neuron. 2021 Jun 15;109(14):2326-2338. doi: 10.1016/j.neuron.2021.05.016

    Executing learned motor behaviors often requires the transformation of sensory cues into patterns of motor commands that generate appropriately timed actions. The cerebellum and thalamus are two key areas involved in shaping cortical output and movement, but the contribution of a cerebellar-thalamocortical pathway to voluntary movement initiation remains poorly understood. Here, we investigated how an auditory "go cue" transforms thalamocortical activity patterns and how these changes relate to movement initiation. Population responses in dentate/interpositus-recipient regions of motor thalamus reflect a time-locked increase in activity immediately prior to movement initiation that is temporally uncoupled from the go cue, indicative of a fixed-latency feedforward motor timing signal. Blocking cerebellar or motor thalamic output suppresses movement initiation, while stimulation triggers movements in a behavioral context-dependent manner. Our findings show how cerebellar output, via the thalamus, shapes cortical activity patterns necessary for learned context-dependent movement initiation.

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    04/16/21 | Neuropixels 2.0: A miniaturized high-density probe for stable, long-term brain recordings.
    Steinmetz NA, Aydın Ç, Lebedeva A, Okun M, Pachitariu M, Bauza M, Beau M, Bhagat J, Böhm C, Broux M, Chen S, Colonell J, Gardner RJ, Karsh B, Kloosterman F, Kostadinov D, Mora-Lopez C, O'Callaghan J, Park J, Putzeys J, Sauerbrei B, van Daal RJ, Vollan AZ, Wang S, Welkenhuysen M, Ye Z, Dudman JT, Dutta B, Hantman AW, Harris KD, Lee AK, Moser EI, O'Keefe J, Renart A, Svoboda K, Häusser M, Haesler S, Carandini M, Harris TD
    Science. 2021 Apr 16;372(6539):. doi: 10.1126/science.abf4588

    Measuring the dynamics of neural processing across time scales requires following the spiking of thousands of individual neurons over milliseconds and months. To address this need, we introduce the Neuropixels 2.0 probe together with newly designed analysis algorithms. The probe has more than 5000 sites and is miniaturized to facilitate chronic implants in small mammals and recording during unrestrained behavior. High-quality recordings over long time scales were reliably obtained in mice and rats in six laboratories. Improved site density and arrangement combined with newly created data processing methods enable automatic post hoc correction for brain movements, allowing recording from the same neurons for more than 2 months. These probes and algorithms enable stable recordings from thousands of sites during free behavior, even in small animals such as mice.

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    10/01/20 | A genetically defined compartmentalized striatal direct pathway for negative reinforcement.
    Xiao X, Deng H, Furlan A, Yang T, Zhang X, Hwang G, Tucciarone J, Wu P, He M, Palaniswamy R, Ramakrishnan C, Ritola K, Hantman A, Deisseroth K, Osten P, Huang ZJ, Li B
    Cell. 2020 Oct 1;181(1):211. doi: 10.1016/j.cell.2020.08.032

    The striosome compartment within the dorsal striatum has been implicated in reinforcement learning and regulation of motivation, but how striosomal neurons contribute to these functions remains elusive. Here, we show that a genetically identified striosomal population, which expresses the Teashirt family zinc finger 1 (Tshz1) and belongs to the direct pathway, drives negative reinforcement and is essential for aversive learning in mice. Contrasting a "conventional" striosomal direct pathway, the Tshz1 neurons cause aversion, movement suppression, and negative reinforcement once activated, and they receive a distinct set of synaptic inputs. These neurons are predominantly excited by punishment rather than reward and represent the anticipation of punishment or the motivation for avoidance. Furthermore, inhibiting these neurons impairs punishment-based learning without affecting reward learning or movement. These results establish a major role of striosomal neurons in behaviors reinforced by punishment and moreover uncover functions of the direct pathway unaccounted for in classic models.

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    09/09/20 | Cell-type specific outcome representation in primary motor cortex.
    Lavzin M, Levy S, Benisty H, Dubin U, Brosh Z, Aeed F, Mensh BD, Schiller Y, Meir R, Barak O, Talmon R, Hantman AW, Schiller J
    Neuron. 2020 Sep 9;107(5):954-71. doi: 10.1016/j.neuron.2020.06.006

    Adaptive movements are critical to animal survival. To guide future actions, the brain monitors different outcomes, including achievement of movement and appetitive goals. The nature of outcome signals and their neuronal and network realization in motor cortex (M1), which commands the performance of skilled movements, is largely unknown. Using a dexterity task, calcium imaging, optogenetic perturbations, and behavioral manipulations, we studied outcome signals in murine M1. We find two populations of layer 2-3 neurons, “success”- and “failure” related neurons that develop with training and report end-result of trials. In these neurons, prolonged responses were recorded after success or failure trials, independent of reward and kinematics. In contrast, the initial state of layer-5 pyramidal tract neurons contains a memory trace of the previous trial’s outcome. Inter-trial cortical activity was needed to learn new task requirements. These M1 reflective layer-specific performance outcome signals, can support reinforcement motor learning of skilled behavior.

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    08/30/20 | Parvalbumin+ and Npas1+ Pallidal neurons have distinct circuit topology and function.
    Pamukcu A, Cui Q, Xenias HS, Berceau BL, Augustine EC, Fan I, Hantman AW, Lerner TN, Boca SM, Chan CS
    Journal of Neuroscience. 2020 Aug 30:
    05/14/20 | Detecting the Starting Frame of Actions in Video
    Kwak IS, Guo J, Hantman A, Branson K, Kriegman D
    2020 IEEE Winter Conference on Applications of Computer Vision (WACV). 2020 May 14:. doi: 10.1109/WACV45572.202010.1109/WACV45572.2020.9093405

    In this work, we address the problem of precisely localizing key frames of an action, for example, the precise time that a pitcher releases a baseball, or the precise time that a crowd begins to applaud. Key frame localization is a largely overlooked and important action-recognition problem, for example in the field of neuroscience, in which we would like to understand the neural activity that produces the start of a bout of an action. To address this problem, we introduce a novel structured loss function that properly weights the types of errors that matter in such applications: it more heavily penalizes extra and missed action start detections over small misalignments. Our structured loss is based on the best matching between predicted and labeled action starts. We train recurrent neural networks (RNNs) to minimize differentiable approximations of this loss. To evaluate these methods, we introduce the Mouse Reach Dataset, a large, annotated video dataset of mice performing a sequence of actions. The dataset was collected and labeled by experts for the purpose of neuroscience research. On this dataset, we demonstrate that our method outperforms related approaches and baseline methods using an unstructured loss.

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    01/16/20 | Cortical pattern generation during dexterous movement is input-driven.
    Sauerbrei BA, Guo J, Cohen JD, Mischiati M, Guo W, Kabra M, Verma N, Mensh B, Branson K, Hantman AW
    Nature. 2020 Jan 16;577(7790):386-91. doi: 10.1038/s41586-019-1869-9

    The motor cortex controls skilled arm movement by sending temporal patterns of activity to lower motor centres. Local cortical dynamics are thought to shape these patterns throughout movement execution. External inputs have been implicated in setting the initial state of the motor cortex, but they may also have a pattern-generating role. Here we dissect the contribution of local dynamics and inputs to cortical pattern generation during a prehension task in mice. Perturbing cortex to an aberrant state prevented movement initiation, but after the perturbation was released, cortex either bypassed the normal initial state and immediately generated the pattern that controls reaching or failed to generate this pattern. The difference in these two outcomes was probably a result of external inputs. We directly investigated the role of inputs by inactivating the thalamus; this perturbed cortical activity and disrupted limb kinematics at any stage of the movement. Activation of thalamocortical axon terminals at different frequencies disrupted cortical activity and arm movement in a graded manner. Simultaneous recordings revealed that both thalamic activity and the current state of cortex predicted changes in cortical activity. Thus, the pattern generator for dexterous arm movement is distributed across multiple, strongly interacting brain regions.

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    09/19/19 | Reconstruction of 1,000 projection neurons reveals new cell types and organization of long-range connectivity in the mouse brain.
    Winnubst J, Bas E, Ferreira TA, Wu Z, Economo MN, Edson P, Arthur BJ, Bruns C, Rokicki K, Schauder D, Olbris DJ, Murphy SD, Ackerman DG, Arshadi C, Baldwin P, Blake R, Elsayed A, Hasan M, Ramirez D, Dos Santos B, Weldon M, Zafar A, Dudman JT, Gerfen CR, Hantman AW, Korff W, Sternson SM, Spruston N, Svoboda K, Chandrashekar J
    Cell. 2019 Sep 19;179(1):268-81. doi: 10.1016/j.cell.2019.07.042

    Neuronal cell types are the nodes of neural circuits that determine the flow of information within the brain. Neuronal morphology, especially the shape of the axonal arbor, provides an essential descriptor of cell type and reveals how individual neurons route their output across the brain. Despite the importance of morphology, few projection neurons in the mouse brain have been reconstructed in their entirety. Here we present a robust and efficient platform for imaging and reconstructing complete neuronal morphologies, including axonal arbors that span substantial portions of the brain. We used this platform to reconstruct more than 1,000 projection neurons in the motor cortex, thalamus, subiculum, and hypothalamus. Together, the reconstructed neurons constitute more than 85 meters of axonal length and are available in a searchable online database. Axonal shapes revealed previously unknown subtypes of projection neurons and suggest organizational principles of long-range connectivity.

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    09/16/19 | A repeated molecular architecture across thalamic pathways.
    Phillips JW, Schulmann A, Hara E, Winnubst J, Liu C, Valakh V, Wang L, Shields BC, Korff W, Chandrashekar J, Lemire AL, Mensh B, Dudman JT, Nelson SB, Hantman AW
    Nature Neuroscience. 2019 Sep 16;22(11):1925-35. doi: 10.1038/s41593-019-0483-3

    The thalamus is the central communication hub of the forebrain and provides the cerebral cortex with inputs from sensory organs, subcortical systems and the cortex itself. Multiple thalamic regions send convergent information to each cortical region, but the organizational logic of thalamic projections has remained elusive. Through comprehensive transcriptional analyses of retrogradely labeled thalamic neurons in adult mice, we identify three major profiles of thalamic pathways. These profiles exist along a continuum that is repeated across all major projection systems, such as those for vision, motor control and cognition. The largest component of gene expression variation in the mouse thalamus is topographically organized, with features conserved in humans. Transcriptional differences between these thalamic neuronal identities are tied to cellular features that are critical for function, such as axonal morphology and membrane properties. Molecular profiling therefore reveals covariation in the properties of thalamic pathways serving all major input modalities and output targets, thus establishing a molecular framework for understanding the thalamus.

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