Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAAReceptors in the Hippocampus

Abstract

Networks of parvalbumin (PV)-expressing basket cells are implicated in synchronizing cortical neurons at various frequencies, through GABAAreceptor-mediated synaptic action. These cells are interconnected by GABAergic synapses and gap junctions, and converge with a different class of cholecystokinin-expressing, PV-negative basket cells onto pyramidal cells. To define the molecular specializations in the synapses of the two basket cell populations, we used quantitative electron microscopic immunogold localization of GABAAreceptors. Synapses formed by PV-positive basket cells on the somata of pyramidal cells had several-fold higher density of α1subunit-containing receptors than synapses made by PV-negative basket cells, most of which were immunonegative. The density of the β2/3subunits was similar in the two populations of synapse, indicating similar overall receptor density. Synapses interconnecting parvalbumin-expressing basket cells contained a 3.6 times higher overall density of GABAAreceptor (β2/3subunits) and 3.2 times higher density of α1subunit labeling compared with synapses formed by boutons of PV-positive basket cells on pyramidal cells. Thus, PV-positive basket cells mainly act through α1subunit-containing GABAAreceptors, but the receptor density depends on the postsynaptic cell type. These observations, together with previously reported enrichment of the α2subunit-containing receptors in synapses made by PV-negative basket cells, indicate that the number and subtypes of GABAAreceptors present in different synapse populations are regulated by both presynaptic and postsynaptic influences. The high number of GABAAreceptors in synapses on basket cells might contribute to the precisely timed phasing of basket cell activity.