Circuit Mechanisms Underlying the Segregation and Integration of Parallel Processing Streams in the Inferior Colliculus

J Neurosci. 2020 Aug 12;40(33):6328-6344. doi: 10.1523/JNEUROSCI.0646-20.2020. Epub 2020 Jul 14.

Abstract

The lateral cortex of the inferior colliculus (LCIC) forms a nexus between diverse multisensory, motor, and neuromodulatory streams. Like other integration hubs, it contains repeated neurochemical motifs with distinct inputs: GABA-rich modules are innervated by somatosensory structures, while auditory inputs to the LCIC target the surrounding extramodular matrix. To investigate potential mechanisms of convergence between these input streams, we used laser photostimulation circuit mapping to interrogate local LCIC circuits in adult mice of both sexes and found that input patterns are highly dependent on cell type (GABAergic/non-GABAergic) and location (module/matrix). At the circuit level, these inputs yield a directional flow of local information, primarily from the matrix to the modules. Further, the two compartments were found to project to distinct targets in the midbrain and thalamus. These data show that, while connectional modularity in the LCIC gives rise to segregated input-output channels, local circuits provide the architecture for integration between these two streams.SIGNIFICANCE STATEMENT Modularity is a widespread motif across the brain involving the segregation of structures into discrete subregions based on dichotomies in neurochemical expression or connectivity. The inferior colliculus is one such modular structure, containing auditory-recipient matrix regions and GABA-rich modules that are innervated by somatosensory inputs. While modularity suggests segregation of processing streams, here we show that local circuits in the inferior colliculus connect the module and matrix regions, providing an avenue for integration of information across compartments.

Keywords: auditory; colliculus; module; photostimulation; somatosensory; thalamus.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Auditory Pathways / cytology
  • Auditory Pathways / physiology*
  • Female
  • GABAergic Neurons / physiology*
  • Inferior Colliculi / cytology
  • Inferior Colliculi / physiology*
  • Male
  • Membrane Potentials
  • Mice, Transgenic
  • Neural Pathways / physiology
  • Neurons / physiology
  • Somatosensory Cortex / cytology
  • Somatosensory Cortex / physiology*