Spatial Profile of Excitatory and Inhibitory Synaptic Connectivity in Mouse Primary Auditory Cortex

J Neurosci. 2012 Apr 18;32(16):5609-19. doi: 10.1523/JNEUROSCI.5158-11.2012.

Abstract

The role of local cortical activity in shaping neuronal responses is controversial. Among other questions, it is unknown how the diverse response patterns reported in vivo-lateral inhibition in some cases, approximately balanced excitation and inhibition (co-tuning) in others-compare to the local spread of synaptic connectivity. Excitatory and inhibitory activity might cancel each other out, or, whether one outweighs the other, receptive field properties might be substantially affected. As a step toward addressing this question, we used multiple intracellular recording in mouse primary auditory cortical slices to map synaptic connectivity among excitatory pyramidal cells and the two broad classes of inhibitory cells, fast-spiking (FS) and non-FS cells in the principal input layer. Connection probability was distance-dependent; the spread of connectivity, parameterized by Gaussian fits to the data, was comparable for all cell types, ranging from 85 to 114 μm. With brief stimulus trains, unitary synapses formed by FS interneurons were stronger than other classes of synapses; synapse strength did not correlate with distance between cells. The physiological data were qualitatively consistent with predictions derived from anatomical reconstruction. We also analyzed the truncation of neuronal processes due to slicing; overall connectivity was reduced but the spatial pattern was unaffected. The comparable spatial patterns of connectivity and relatively strong excitatory-inhibitory interconnectivity are consistent with a theoretical model where either lateral inhibition or co-tuning can predominate, depending on the structure of the input.

Publication types

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

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Animals, Newborn
  • Auditory Cortex / cytology*
  • Auditory Cortex / physiology*
  • Auditory Pathways / physiology
  • Axons / physiology
  • Biophysics
  • Brain Mapping
  • Dendrites / physiology
  • Electric Stimulation
  • Glutamate Decarboxylase / genetics
  • Glutamate Decarboxylase / metabolism
  • Green Fluorescent Proteins / genetics
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / physiology
  • Mice
  • Mice, Transgenic
  • Nerve Net / physiology
  • Neural Inhibition / physiology*
  • Neurons / cytology
  • Neurons / physiology*
  • Normal Distribution
  • Patch-Clamp Techniques
  • Synapses / physiology*
  • Thalamus / cytology
  • Thalamus / physiology

Substances

  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1