Context-dependent limb movement encoding in neuronal populations of motor cortex

Omlor, Wolfgang; Sipilä, Pia; Wahl, Anna-Sophia; Lütcke, Henry; Laurenczy, Balazs; Chen, I‐Wen; Sumanovski, Lazar T.; Hoff, Marcel van ‘t; Bethge, Philipp; Voigt, Fabian F.

doi:10.1101/588129

Cited by 10 publications

(13 citation statements)

References 77 publications

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“…This suggests that task context may adjust the contribution of relevant task parameters in determining the population activity, thus serving as a population encoding of differing contextual information for similar movement topologies. The results are consistent with previous findings showing context-dependent modulation of cortical encoding during texture discrimination in task vs. no-task conditions and grasping behavior with regular vs. irregular ladder wheels (49,50).…”

Section: Neuronal Population Encoding Of Task Parameters Reveals Contsupporting

confidence: 92%

Multiple regions of primate orofacial sensorimotor cortex encode bite force and gape

Arce-McShane¹,

Sessle

Ram³

et al. 2020

Preprint

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The precise control of bite force and gape is vital for effective breakdown and manipulation of food inside the oral cavity during feeding. Yet the role of the orofacial sensorimotor cortex (OSMcx) in the control of bite force and gape is still largely unknown. The aim of this study was to elucidate how individual neurons and populations of neurons in multiple regions of OSMcx differentially encode bite force and gape when subjects (Macaca mulatta) generated different levels of bite force at varying gapes. We examined neuronal activity recorded simultaneously from three microelectrode arrays implanted chronically in the primary motor (MIo), primary somatosensory (SIo), and cortical masticatory (CMA) areas of OSMcx. We used generalized linear models to evaluate encoding properties of individual neurons and utilized dimensionality reduction techniques to decompose population activity into components related to specific task parameters. Individual neurons encoded bite force more strongly than gape in all three OSMCx areas although bite force was a better predictor of spiking activity in MIo versus SIo. Population activity differentiated between levels of bite force and gape while preserving task-independent temporal modulation across the behavioral trial. While activation patterns of neuronal populations were comparable across OSMCx areas, the total variance explained by task parameters was context-dependent and differed across areas. These findings suggest that the cortical control of gape may rely on computations at the population level whereas the strong encoding of bite force at the individual neuron level allows for the precise and rapid control of bite force.Significance StatementBiting a piece off an apple requires precise sensorimotor control and coordination of bite force and gape by multiple brain regions. The cortical representations of bite force and gape by individual neurons and large populations of neurons across connected motor and somatosensory areas in orofacial cortex is unknown. Here we showed that bite force was more strongly encoded than gape by individual neurons in primary motor, somatosensory, and cortical masticatory areas. Moreover, bite force was more effectively represented in motor versus somatosensory cortices. At the population level, bite force and gape were distinguishable particularly when gape was randomized from trial-to-trial. The results are important for understanding neurophysiological processes underlying masticatory dysfunctions that may occur in aging, stroke, and Alzheimer’s disease.

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Section: Neuronal Population Encoding Of Task Parameters Reveals Contsupporting

confidence: 92%

Multiple regions of primate orofacial sensorimotor cortex encode bite force and gape

Arce-McShane¹,

Sessle

Ram³

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…The ability to alter the sequencing of actions to match the current environmental context is observed across animals and behaviors, including for social interactions [46,47,48,49,50]. Here, we provide insights into the underlying circuit mechanisms by focusing on song production in two contexts in Drosophila melanogaster, near versus far from a female.…”

Section: Discussionmentioning

confidence: 99%

Flexible Circuit Mechanisms for Context-Dependent Song Sequencing

Roemschied

et al. 2021

Preprint

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Many sequenced behaviors, including locomotion, reaching, and vocalization, are patterned differently in different contexts, enabling animals to adjust to their current environments. However, how contextual information shapes neural activity to flexibly alter the patterning of actions is not yet understood. Prior work indicates such flexibility could be achieved via parallel motor circuits, with differing sensitivities to sensory context [1, 2, 3]; instead we demonstrate here how a single neural pathway operates in two different regimes dependent on recent sensory history. We leverage the Drosophila song production system [4] to investigate the neural mechanisms that support male song sequence generation in two contexts: near versus far from the female. While previous studies identified several song production neurons[5, 6, 7, 8], how these neurons are organized to mediate song patterning was unknown. We find that male flies sing ‘simple’ trains of only one syllable or mode far from the female but complex song sequences consisting of alternations between modes when near to her. We characterize the male song circuit from the brain to the ventral nerve cord (VNC), and find that the VNC song pre-motor circuit is shaped by two key computations: mutual inhibition and rebound excitability [9] between nodes driving the two modes of song. Weak sensory input to a direct brain-to-VNC excitatory pathway (via pC2 brain and pIP10 descending neurons) drives simple song far from the female. Strong sensory input to the same pathway enables complex song production via simultaneous recruitment of P1a neuron-mediated disinhibition of the VNC song pre-motor circuit. Thus, proximity to the female effectively unlocks motor circuit dynamics in the correct sensory context. We construct a compact circuit model to demonstrate that these few computations are sufficient to replicate natural context-dependent song dynamics. These results have broad implications for neural population-level models of context-dependent behavior [10] and highlight that canonical circuit motifs [11, 12, 13] can be combined in novel ways to enable circuit flexibility required for dynamic communication.

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“…In mouse motor cortex, local pyramidal neurons providing input to the proximal dendrites exhibit elevated activity for several seconds associated with movement (3-100 Hz) (Li et al, 2015;Omlor et al, 2019;Sauerbrei et al, 2020;Sreenivasan et al, 2016). Thalamic neurons providing ascending input are also active (4-15 Hz) during these periods (Catanese and Jaeger, 2021;Poulet et al, 2012;Takahashi et al, 2021).…”

Section: Resultsmentioning

confidence: 99%

Context-dependent limb movement encoding in neuronal populations of motor cortex

Cited by 10 publications

References 77 publications

Multiple regions of primate orofacial sensorimotor cortex encode bite force and gape

Multiple regions of primate orofacial sensorimotor cortex encode bite force and gape

Flexible Circuit Mechanisms for Context-Dependent Song Sequencing

Input rate encoding and gain control in dendrites of neocortical pyramidal neurons

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