Kinetic features dictate sensorimotor alignment in the superior colliculus

Nature. 2024 Jul;631(8020):378-385. doi: 10.1038/s41586-024-07619-2. Epub 2024 Jul 3.

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.

MeSH terms

  • Animals
  • Female
  • Goals
  • Kinetics
  • Male
  • Models, Neurological*
  • Motor Neurons / physiology
  • Movement* / physiology
  • Nerve Net / cytology
  • Nerve Net / physiology
  • Photic Stimulation
  • Psychomotor Performance / physiology
  • Reproducibility of Results
  • Superior Colliculi* / cytology
  • Superior Colliculi* / physiology
  • Visual Perception* / physiology