Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus
- PMID: 11784700
- DOI: 10.1016/s0306-4522(01)00440-7
Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus
Abstract
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.
Similar articles
-
GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat.Eur J Neurosci. 2004 Feb;19(3):552-69. doi: 10.1111/j.0953-816x.2003.03091.x. Eur J Neurosci. 2004. PMID: 14984406
-
Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus.J Comp Neurol. 2002 Feb 18;443(4):346-67. doi: 10.1002/cne.10118. J Comp Neurol. 2002. PMID: 11807843
-
Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro.J Physiol. 1998 Feb 1;506 ( Pt 3)(Pt 3):755-73. doi: 10.1111/j.1469-7793.1998.755bv.x. J Physiol. 1998. PMID: 9503336 Free PMC article.
-
GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus.Eur J Neurosci. 2009 Sep;30(6):947-57. doi: 10.1111/j.1460-9568.2009.06913.x. Epub 2009 Sep 4. Eur J Neurosci. 2009. PMID: 19735288 Review.
-
Neocortical inhibitory system.Folia Biol (Praha). 2009;55(6):201-17. Folia Biol (Praha). 2009. PMID: 20163769 Review.
Cited by
-
Ventral hippocampal cholecystokinin interneurons gate contextual reward memory.iScience. 2024 Jan 9;27(2):108824. doi: 10.1016/j.isci.2024.108824. eCollection 2024 Feb 16. iScience. 2024. PMID: 38303709 Free PMC article.
-
Local and long-range GABAergic circuits in hippocampal area CA1 and their link to Alzheimer's disease.Front Neural Circuits. 2023 Sep 29;17:1223891. doi: 10.3389/fncir.2023.1223891. eCollection 2023. Front Neural Circuits. 2023. PMID: 37841892 Free PMC article. Review.
-
Structural Organization of Perisomatic Inhibition in the Mouse Medial Prefrontal Cortex.J Neurosci. 2023 Oct 18;43(42):6972-6987. doi: 10.1523/JNEUROSCI.0432-23.2023. Epub 2023 Aug 28. J Neurosci. 2023. PMID: 37640552 Free PMC article.
-
Hippocampal GABAergic interneurons and memory.Neuron. 2023 Oct 18;111(20):3154-3175. doi: 10.1016/j.neuron.2023.06.016. Epub 2023 Jul 18. Neuron. 2023. PMID: 37467748 Free PMC article. Review.
-
Lateral entorhinal cortex inputs modulate hippocampal dendritic excitability by recruiting a local disinhibitory microcircuit.Cell Rep. 2023 Jan 31;42(1):111962. doi: 10.1016/j.celrep.2022.111962. Epub 2023 Jan 4. Cell Rep. 2023. PMID: 36640337 Free PMC article.
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Miscellaneous