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Kinetic features dictate sensorimotor alignment in the superior colliculus

Ana González-Rueda (), Kristopher Jensen, Mohammadreza Noormandipour, Daniel Malmazet, Jonathan Wilson, Ernesto Ciabatti, Jisoo Kim, Elena Williams, Jasper Poort, Guillaume Hennequin and Marco Tripodi ()
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Ana González-Rueda: MRC Laboratory of Molecular Biology
Kristopher Jensen: University of Cambridge
Mohammadreza Noormandipour: University of Cambridge
Daniel Malmazet: MRC Laboratory of Molecular Biology
Jonathan Wilson: MRC Laboratory of Molecular Biology
Ernesto Ciabatti: MRC Laboratory of Molecular Biology
Jisoo Kim: University of Cambridge
Elena Williams: MRC Laboratory of Molecular Biology
Jasper Poort: University of Cambridge
Guillaume Hennequin: MRC Laboratory of Molecular Biology
Marco Tripodi: MRC Laboratory of Molecular Biology

Nature, 2024, vol. 631, issue 8020, 378-385

Abstract: Abstract The execution of goal-oriented behaviours requires a spatially coherent alignment between sensory and motor maps. The current model for sensorimotor transformation in the superior colliculus relies on the topographic mapping of static spatial receptive fields onto movement endpoints1–6. Here, to experimentally assess the validity of this canonical static model of alignment, we dissected the visuo-motor network in the superior colliculus and performed in vivo intracellular and extracellular recordings across layers, in restrained and unrestrained conditions, to assess both the motor and the visual tuning of individual motor and premotor neurons. We found that collicular motor units have poorly defined visual static spatial receptive fields and respond instead to kinetic visual features, revealing the existence of a direct alignment in vectorial space between sensory and movement vectors, rather than between spatial receptive fields and movement endpoints as canonically hypothesized. We show that a neural network built according to these kinetic alignment principles is ideally placed to sustain ethological behaviours such as the rapid interception of moving and static targets. These findings reveal a novel dimension of the sensorimotor alignment process. By extending the alignment from the static to the kinetic domain this work provides a novel conceptual framework for understanding the nature of sensorimotor convergence and its relevance in guiding goal-directed behaviours.

Date: 2024
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DOI: 10.1038/s41586-024-07619-2

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