Connectivity of GABAergic calretinin-immunoreactive neurons in rat primary visual cortex

Cereb Cortex. 1999 Oct-Nov;9(7):683-96. doi: 10.1093/cercor/9.7.683.

Abstract

In rat visual cortex neurons that are immunoreactive for the calcium-binding protein calretinin (CR+) constitute a distinct family which accounts for 17% of gamma-aminobutyric acid (GABA)-expressing cells. It is not clear, however, (i) whether CR is expressed exclusively in GABAergic neurons and (ii) how CR+ neurons are incorporated into neuronal circuits of rat visual cortex. To address these questions we studied synaptic relationships of CR+ neurons with GABA+ and GABA- elements in the neuropil of rat primary visual cortex (area 17). All CR+ neurons are nonpyramidal cells with smooth or sparsely spiny and often beaded dendrites. Of all CR+ neurons, 56% are located in layers 1 and 2/3. In layer 2/3, most CR+ neurons are bipolar-shaped and have vertically oriented dendrites. Many ascending dendritic branches reach layer 1 where they run parallel to pial surface. CR+ axons are thin, highly branched near the cell body and often send descending collaterals to layers 5 and 6. Double immunofluorescence labeling revealed GABA in 94% of CR+ cell bodies in layer 2/3. Electron microscopic analysis shows that all CR+ axon terminals contain elongated vesicles and form symmetric synapses. Postembedding staining shows that 98% of CR+ terminals are GABA+. GABA-immunoreactivity is also present in somata and thick dendrites of CR+ neurons but many thin dendrites are GABA-. CR+ somata, dendrites and axon terminals are enriched in mitochondria. Somata and thick CR+ dendrites are densely innervated. At least 68% of the targets of CR+ terminals in layer 2/3 are GABA+ and > or = 50% of these are other CR+ neurons. The remainder (32%) of targets of CR+ terminals are thin dendrites of GABA- cells. In contrast, in layers 5 and 6, 60% of CR+ terminals form synapses with GABA- somatic profiles. The preferential interactions of layer 2/3 CR+ neurons with GABAergic neurons, and with CR+ neurons in particular, suggests that these cells play a role in the inhibition of inhibitory neurons of the same layer. Through these interactions CR+ cells may reduce inhibition of pyramidal cells in layers 2/3, 5 and 6 and thus disinhibit a column of neurons.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Calbindin 2
  • Dendrites / chemistry
  • Dendrites / ultrastructure
  • Fluorescent Antibody Technique
  • Microscopy, Electron
  • Neurons / chemistry*
  • Neurons / ultrastructure
  • Presynaptic Terminals / chemistry
  • Presynaptic Terminals / ultrastructure
  • Rats
  • S100 Calcium Binding Protein G / analysis*
  • Visual Cortex / chemistry
  • Visual Cortex / cytology*
  • Visual Pathways
  • gamma-Aminobutyric Acid / analysis*

Substances

  • Calb2 protein, rat
  • Calbindin 2
  • S100 Calcium Binding Protein G
  • gamma-Aminobutyric Acid