Navigation requires steering and propulsion, but how spinal circuits contribute to direction control during ongoing locomotion is not well understood. Here, we use drifting vertical gratings to evoke directed “fictive” swimming in intact but immobilized larval zebrafish while performing electrophysiological recordings from spinal neurons. We find that directed swimming involves unilateral changes in the duration of motor output and increased recruitment of motor neurons, without impacting the timing of spiking across or along the body. Voltage-clamp recordings from motor neurons reveal increases in phasic excitation and inhibition on the side of the turn. Current-clamp recordings from premotor interneurons that provide phasic excitation or inhibition reveal two types of recruitment patterns. A direction-agnostic pattern with balanced recruitment on the turning and nonturning sides is primarily observed in excitatory V2a neurons with ipsilateral descending axons, while a direction-sensitive pattern with preferential recruitment on the turning side is dominated by V2a neurons with ipsilateral bifurcating axons. Inhibitory V1 neurons are also divided into direction-sensitive and direction-agnostic subsets, although there is no detectable morphologic distinction. Our findings support the modular control of steering and propulsion by spinal premotor circuits, where recruitment of distinct subsets of excitatory and inhibitory interneurons provide adjustments in direction while on the move.
This content will become publicly available on October 1, 2024
Visual control of steps is critical for daily living, however, how it is achieved is not well understood. Here, we analyzed how neurons in the premotor cortex respond to the demand for visual control of steps on a complex surface. We conclude that premotor cortex neurons participate in the cortical network supporting visual control of steps by modifying the phase, intensity, and salience of their firing activity.
more » « less- Award ID(s):
- 1912557
- NSF-PAR ID:
- 10482024
- Publisher / Repository:
- American Physiological Society
- Date Published:
- Journal Name:
- Journal of Neurophysiology
- Volume:
- 130
- Issue:
- 4
- ISSN:
- 0022-3077
- Page Range / eLocation ID:
- 838 to 860
- Subject(s) / Keyword(s):
- accuracy locomotion PTN vision walking
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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SIGNIFICANCE STATEMENT Spinal circuits play an essential role in coordinating movements during locomotion. However, it is unclear how they participate in adjustments in direction that do not interfere with coordination. Here we have developed a system using larval zebrafish that allows us to directly record electrical signals from spinal neurons during “fictive” swimming guided by visual cues. We find there are subsets of spinal interneurons for coordination and others that drive unilateral asymmetries in motor neuron recruitment for direction control. Our findings suggest a modular organization of spinal premotor circuits that enables uninterrupted adjustments in direction during ongoing locomotion. -
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Abstract Objective. Sensorimotor decisions require the brain to process external information and combine it with relevant knowledge prior to actions. In this study, we explore the neural predictors of motor actions in a novel, realistic driving task designed to study decisions while driving.Approach. Through a spatiospectral assessment of functional connectivity during the premotor period, we identified the organization of visual cortex regions of interest into a distinct scene processing network. Additionally, we identified a motor action selection network characterized by coherence between the anterior cingulate cortex (ACC) and dorsolateral prefrontal cortex (DLPFC).Main results. We show that steering behavior can be predicted from oscillatory power in the visual cortex, DLPFC, and ACC. Power during the premotor periods (specific to the theta and beta bands) correlates with pupil-linked arousal and saccade duration.Significance. We interpret our findings in the context of network-level correlations with saccade-related behavior and show that the DLPFC is a key node in arousal circuitry and in sensorimotor decisions. -
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This paper offers a theory for the origin of direction selectivity (DS) in the macaque primary visual cortex, V1. DS is essential for the perception of motion and control of pursuit eye movements. In the macaque visual pathway, neurons with DS first appear in V1, in the Simple cell population of the Magnocellular input layer 4Cα. The lateral geniculate nucleus (LGN) cells that project to these cortical neurons, however, are not direction selective. We hypothesize that DS is initiated in feed-forward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of 1) different visual response dynamics of ON and OFF LGN cells and 2) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that, together with item 2, produce distinct response time courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Cα in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broadband in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.
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