Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus.

Abstract

To investigate the electrophysiological properties, synaptic connections, and anatomy of individual parvalbumin-immunoreactive (PV-IR) and cholecystokinin-immunoreactive (CCK-IR) interneurones in CA1, dual intracellular recordings using biocytin-filled microelectrodes in slices of adult rat hippocampus were combined with fluorescence labelling of PV- and CCK-containing cells. Of 36 PV-IR cells, 29 were basket cells, with most of their axonal arbours in the stratum pyramidale (SP). Six were bistratified cells with axons ramifying throughout stratum oriens (SO) and stratum radiatum (SR). One was a putative axo-axonic cell with an axonal arbour confined to half of the SP and a narrow adjacent region of the SO. Of 27 CCK-IR neurones, 13 were basket cells, with most of their axonal arbours in the SP, and included basket cells with somata in the SP (6), SO (3), and SR (2) and at the border between the stratum lacunosum-moleculare (SLM) and the SR (2). In addition, several dendrite-targeting cell classes expressed CCK-IR: 4 of 9 bistratified cells with axons ramifying in the SO and SR; all five Schaffer-associated cells whose axons ramified extensively in the SR; both cells classified as quadrilaminar because their axons ramified in the SO, SP, SR, and SLM; one SO-SO cell whose dendritic and axonal arbours were contained within the SO; and one perforant path-associated cell with axonal and dendritic arbours within the distal SR and SLM. The majority (31 of 36) of PV-IR neurones recorded were fast-spiking, and most fast-spiking cells tested (25 of 29 basket, 1 axo-axonic, and 5 of 6 bistratified cells) were PV-IR. However, 1 of 6 regular-spiking basket, 1 of 4 regular-spiking bistratified, and 3 of 5 burst-firing basket cells were also PV-IR. In contrast, the majority (17 of 27) of the CCK-IR neurones recorded were regular-spiking, 3 were burst-firing, and 7 were fast-spiking. These data confirm that the majority of PV-IR and CCK-IR axon terminals innervate proximal portions of CA1 pyramidal cells. Most PV-IR cells are fast-spiking, whereas most CCK-IR cells are regular-spiking. In both neurochemical classes basket cells predominate, but both groups included subpopulations of dendrite-targeting cells. Despite these similarities, the two populations exhibited very different somatic distributions, and each contained cellular morphologies not represented in the other.