Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus

• Published in: Neuroscience 2002-01, Vol.109 (1), p.63-80
• Main Authors: Cope, D.W, Maccaferri, G, Márton, L.F, Roberts, J.D.B, Cobden, P.M, Somogyi, P
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Aging - metabolism; Animals; Animals, Newborn; Axons - metabolism; Axons - ultrastructure; Biological and medical sciences; calbindin; Calbindins; Central nervous system; Central neurotransmission. Neuromudulation. Pathways and receptors; cholecystokinin; Cholecystokinin - metabolism; cortex; Fundamental and applied biological sciences. Psychology; GABA; gamma-Aminobutyric Acid - metabolism; Hippocampus - cytology; Hippocampus - growth & development; Hippocampus - metabolism; Immunohistochemistry; inhibition; Interneurons - cytology; Interneurons - metabolism; Lysine - analogs & derivatives; Male; Neural Inhibition - physiology; Organ Culture Techniques; Pyramidal Cells - cytology; Pyramidal Cells - metabolism; Rats; Rats, Wistar; S100 Calcium Binding Protein G - metabolism; Synaptic Transmission - physiology; Vertebrates: nervous system and sense organs
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/S0306-4522(01)00440-7

Two types of GABAergic interneurone are known to express cholecystokinin-related peptides in the isocortex: basket cells, which preferentially innervate the somata and proximal dendrites of pyramidal cells; and double bouquet cells, which innervate distal dendrites and dendritic spines. In the hippocampus, cholecystokinin immunoreactivity has only been reported in basket cells. However, at least eight distinct GABAergic interneurone types terminate in the dendritic domain of CA1 pyramidal cells, some of them with as yet undetermined neurochemical characteristics. In order to establish whether more than one population of cholecystokinin-expressing interneurone exist in the hippocampus, we have performed whole-cell current clamp recordings from interneurones located in the stratum radiatum of the hippocampal CA1 region of developing rats. Recorded neurones were filled with biocytin to reveal their axonal targets, and were tested for the presence of pro-cholecystokinin immunoreactivity. The results show that two populations of cholecystokinin-immunoreactive interneurones exist in the CA1 area ( n=15 positive cells). Cholecystokinin-positive basket cells (53%) preferentially innervate stratum pyramidale and adjacent strata oriens and radiatum. A second population of cholecystokinin-positive cells, previously described as Schaffer collateral-associated interneurones [Vida et al. (1998) J. Physiol. 506, 755–773], have axons that ramify almost exclusively in strata radiatum and oriens, overlapping with the Schaffer collateral/commissural pathway originating from CA3 pyramidal cells. Two of seven of the Schaffer collateral-associated cells were also immunopositive for calbindin. Soma position and orientation in stratum radiatum, the number and orientation of dendrites, and the passive and active membrane properties of the two cell populations are only slightly different. In addition, in stratum radiatum and its border with lacunosum of perfusion-fixed hippocampi, 31.6±3.8% (adult) or 26.8±2.9% (postnatal day 17–20) of cholecystokinin-positive cells were also immunoreactive for calbindin. Therefore, at least two populations of pro-cholecystokinin-immunopositive interneurones, basket and Schaffer collateral-associated cells, exist in the CA1 area of the hippocampus, and are probably homologous to cholecystokinin-immunopositive basket and double bouquet cells in the isocortex. It is not known if the GABAergic terminals of double bouquet cells are co-aligned with spec