Cortical inputs innervate calbindin-immunoreactive interneurons of the rat basolateral amygdaloid complex

J Comp Neurol. 2014 Jun 1;522(8):1915-28. doi: 10.1002/cne.23511.

Abstract

The present study was undertaken to shed light on the synaptic organization of the rat basolateral amygdala (BLA). The BLA contains multiple types of GABAergic interneurons that are differentially connected with extrinsic afferents and other BLA cells. Previously, it was reported that parvalbumin immunoreactive (PV(+) ) interneurons receive strong excitatory inputs from principal BLA cells but very few cortical inputs, implying a prevalent role in feedback inhibition. However, because prior physiological studies indicate that cortical afferents do trigger feedforward inhibition in principal cells, the present study aimed to determine whether a numerically important subtype of interneurons, expressing calbindin (CB(+) ), receives cortical inputs. Rats received injections of the anterograde tracer Phaseolus vulgaris-leucoagglutinin (PHAL) in the perirhinal cortex or adjacent temporal neocortex. Light and electron microscopic observations of the relations between cortical inputs and BLA neurons were performed in the lateral (LA) and basolateral (BL) nuclei. Irrespective of the injection site (perirhinal or temporal neocortex) and target nucleus (LA or BL), ~90% of cortical axon terminals formed asymmetric synapses with dendritic spines of principal BLA neurons, while 10% contacted the dendritic shafts of presumed interneurons, half of which were CB(+) . Given the previously reported pattern of CB coexpression among GABAergic interneurons of the BLA, these results suggest that a subset of PV-immunonegative cells that express CB, most likely the somatostatin-positive interneurons, are important mediators of cortically evoked feedforward inhibition in the BLA.

Keywords: amygdala; calbindin; electron microscopy; feedforward inhibition; tract-tracing.

Publication types

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

MeSH terms

  • Amygdala / chemistry
  • Amygdala / metabolism*
  • Amygdala / ultrastructure
  • Animals
  • Calbindins / analysis
  • Calbindins / biosynthesis*
  • Cerebral Cortex / chemistry
  • Cerebral Cortex / metabolism*
  • Cerebral Cortex / ultrastructure
  • Humans
  • Interneurons / chemistry
  • Interneurons / metabolism*
  • Interneurons / ultrastructure
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Calbindins