Lack of Evidence for Stereotypical Direction Columns in the Mouse Superior Colliculus

J Neurosci. 2021 Jan 20;41(3):461-473. doi: 10.1523/JNEUROSCI.1155-20.2020. Epub 2020 Nov 19.

Abstract

Neurons in the visual system can be spatially organized according to their response properties such as receptive field location and feature selectivity. For example, the visual cortex of many mammalian species contains orientation and direction columns where neurons with similar preferences are clustered. Here, we examine whether such a columnar structure exists in the mouse superior colliculus (SC), a prominent visual center for motion processing. By performing large-scale physiological recording and two-photon calcium imaging in adult male and female mice, we show that direction-selective neurons in the mouse SC are not organized into stereotypical columns as a function of their preferred directions, although clusters of similarly tuned neurons are seen in a minority of mice. Nearby neurons can prefer similar or opposite directions in a largely position-independent manner. This finding holds true regardless of animal state (anesthetized vs awake, running vs stationary), SC depth (most superficial lamina vs deeper in the SC), research technique (calcium imaging vs electrophysiology), and stimulus type (drifting gratings vs moving dots, full field vs small patch). Together, these results challenge recent reports of region-specific organizations in the mouse SC and reveal how motion direction is represented in this important visual center.

Keywords: columnar organization; direction selectivity; mouse visual system; silicon probes; superior colliculus; two-photon imaging.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anesthesia
  • Animals
  • Electrophysiological Phenomena
  • Female
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Motion Perception
  • Neuroimaging
  • Photic Stimulation
  • Running / physiology
  • Superior Colliculi / cytology
  • Superior Colliculi / diagnostic imaging
  • Superior Colliculi / physiology*
  • Visual Pathways / diagnostic imaging
  • Visual Pathways / physiology*
  • Wakefulness