Columnar connectivity and laminar processing in cat primary auditory cortex

PLoS One. 2010 Mar 3;5(3):e9521. doi: 10.1371/journal.pone.0009521.

Abstract

Background: Radial intra- and interlaminar connections form a basic microcircuit in primary auditory cortex (AI) that extracts acoustic information and distributes it to cortical and subcortical networks. Though the structure of this microcircuit is known, we do not know how the functional connectivity between layers relates to laminar processing.

Methodology/principal findings: We studied the relationships between functional connectivity and receptive field properties in this columnar microcircuit by simultaneously recording from single neurons in cat AI in response to broadband dynamic moving ripple stimuli. We used spectrotemporal receptive fields (STRFs) to estimate the relationship between receptive field parameters and the functional connectivity between pairs of neurons. Interlaminar connectivity obtained through cross-covariance analysis reflected a consistent pattern of information flow from thalamic input layers to cortical output layers. Connection strength and STRF similarity were greatest for intralaminar neuron pairs and in supragranular layers and weaker for interlaminar projections. Interlaminar connection strength co-varied with several STRF parameters: feature selectivity, phase locking to the stimulus envelope, best temporal modulation frequency, and best spectral modulation frequency. Connectivity properties and receptive field relationships differed for vertical and horizontal connections.

Conclusions/significance: Thus, the mode of local processing in supragranular layers differs from that in infragranular layers. Therefore, specific connectivity patterns in the auditory cortex shape the flow of information and constrain how spectrotemporal processing transformations progress in the canonical columnar auditory microcircuit.

Publication types

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

MeSH terms

  • Acoustic Stimulation*
  • Animals
  • Auditory Cortex / physiology*
  • Auditory Perception / physiology
  • Cats
  • Computer Simulation
  • Electrophysiology
  • Models, Neurological
  • Models, Statistical
  • Neurons / metabolism
  • Neurons / pathology
  • Synapses
  • Thalamus / physiology
  • Time Factors