Postsynaptic targets of GABAergic basal forebrain projections to the basolateral amygdala

Neuroscience. 2011 Jun 2:183:144-59. doi: 10.1016/j.neuroscience.2011.03.027. Epub 2011 Mar 22.

Abstract

Recent studies indicate that the basolateral amygdala, like the neocortex and hippocampus, receives GABAergic inputs from the basal forebrain in addition to the well-established cholinergic inputs. Since the neuronal targets of these inputs have yet to be determined, it is difficult to predict the functional significance of this innervation. The present study addressed this question in the rat by employing anterograde tract tracing combined with immunohistochemistry at the light and electron microscopic levels of analysis. Amygdalopetal axons from the basal forebrain mainly targeted the basolateral nucleus (BL) of the amygdala. The morphology of these axons was heterogeneous and included GABAergic axons that contained vesicular GABA transporter protein (VGAT). These axons, designated type 1, exhibited distinctive large axonal varicosities that were typically clustered along the length of the axon. Type 1 axons formed multiple contacts with the cell bodies and dendrites of parvalbumin-containing (PV+) interneurons, but relatively few contacts with calretinin-containing and somatostatin-containing interneurons. At the ultrastructural level of analysis, the large terminals of type 1 axons exhibited numerous mitochondria and were densely packed with synaptic vesicles. Individual terminals formed broad symmetrical synapses with BL PV+ interneurons, and often formed additional symmetrical synapses with BL pyramidal cells. Some solitary type 1 terminals formed symmetrical synapses solely with BL pyramidal cells. These results suggest that GABAergic neurons of the basal forebrain provide indirect disinhibition, as well as direct inhibition, of BL pyramidal neurons. The possible involvement of these circuits in rhythmic oscillations related to emotional learning, attention, and arousal is discussed.

Publication types

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

MeSH terms

  • Amygdala / physiology*
  • Amygdala / ultrastructure
  • Animals
  • Axons / metabolism*
  • Axons / ultrastructure
  • Biotin / analogs & derivatives
  • Biotin / metabolism
  • Calbindins
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism
  • Dextrans / metabolism
  • Efferent Pathways / physiology
  • Male
  • Microscopy, Immunoelectron
  • Phytohemagglutinins / metabolism
  • Prosencephalon / metabolism*
  • Prosencephalon / ultrastructure
  • Rats
  • Rats, Sprague-Dawley
  • S100 Calcium Binding Protein G / metabolism
  • Synapses / metabolism
  • Synapses / ultrastructure
  • Vesicular Inhibitory Amino Acid Transport Proteins / metabolism
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Calbindins
  • Dextrans
  • Phytohemagglutinins
  • S100 Calcium Binding Protein G
  • Slc32a1 protein, rat
  • Vesicular Inhibitory Amino Acid Transport Proteins
  • biotinylated dextran amine
  • leukoagglutinins, plants
  • gamma-Aminobutyric Acid
  • Biotin
  • Calcium-Calmodulin-Dependent Protein Kinases