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 Vol. 109; no. 1; pp. 63 - 80
• Main Authors: Cope, D.W, Maccaferri, G, Márton, L.F, Roberts, J.D.B, Cobden, P.M, Somogyi, P
• Format: Journal Article
• Language: English
• Published: Oxford Elsevier Ltd 01-01-2002; Elsevier
• 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; cholecystokinin; TBS, Tris-buffered saline; mAHP, medium-duration after-hyperpolarisation; calbindin; HRP, horseradish peroxidase; P, postnatal day; PV, parvalbumin; V h, holding membrane potential; CB1, cannabinoid receptor type 1; cortex; ADP, after-depolarisation; CCK, cholecystokinin; HEPES, N-(2-hydroxyethyl)piperazine- N′-(2-ethanesulphonic acid); R N, input resistance; inhibition; EPSPs, excitatory postsynaptic potentials; fAHP, fast after-hyperpolarisation; ISI, inter-spike interval; AHP, after-hyperpolarisation; AMCA, 7-amino-4-methylcoumarin-3-acetic acid; aCSF, artificial cerebrospinal fluid; VIP, vasoactive intestinal polypeptide; GABA; τ m, membrane time constant; V m, resting membrane potential; IPSPs, inhibitory postsynaptic potentials; Calbindin; Calcium; Rat; Rodentia; Central nervous system; Neuropeptide; Interneuron; Binding protein; Vertebrata; Mammalia; Cholecystokinin; Pyramidal neuron; Hippocampus; Brain (vertebrata); Gabaergic neuron
• 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 specific glutamatergic inputs. However, in the hippocampal CA1 area, it is clear that the terminals of Schaffer collateral-associated cells are co-stratified with the glutamatergic input from the CA3 area, with as yet unknown functional consequences. The division of the postsynaptic neuronal surface by two classes of GABAergic cell expressing cholecystokinin in both the hippocampus and isocortex provides further evidence for the uniform synaptic organisation of the cerebral cortex.