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

Cope, D.W, Maccaferri, G, Márton, L.F, Roberts, J.D.B, Cobden, P.M, Somogyi, P·2002·Neuroscience
DOI 10.1016/s0306-4522(01)00440-7
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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.

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Crossref · 10.1016/s0306-4522(01)00440-7

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117 of 117 references verified0 citation errors · 0 not checkable

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  • The defining anatomical feature of CCKBCs is preferential perisomatic axonal targeting within stratum pyramidale to surround the soma and proximal dendrites of pyramidal cells.

    “Like PVBCs, the defining anatomical feature of CCKBCs is preferential perisomatic axonal targeting within s.p. to surround the soma and proximal dendrites of pyramidal cells (FIGURE 2E) (224, 352, 584, 1036, 1172).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [224]

  • While the majority of CCKBC somas reside within stratum radiatum, with a significant concentration at the stratum radiatum/stratum lacunosum moleculare border, substantial numbers can also be found in stratum pyramidale and stratum oriens.

    “While the majority of CCKBC somas reside within s.r., with a significant concentration at the s.r/s.l.m. border, substantial numbers can also be found in s.p. and s.o. (224, 258, 340, 584, 654, 1172).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [224]

  • A minority (~8%) of CCK-expressing dendrite targeting cell terminals innervate other interneurons.

    “All CCK-expressing dendrite targeting cells dominantly target principal cell postsynaptic targets with ~6 synapses per connection; however, a minority of terminals (~8%) innervate other interneurons (102, 224, 584, 1172).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [224]

  • Additional molecular markers commonly associated with hippocampal and neocortical CCK-expressing dendrite targeting interneurons are calbindin (CB) (hippocampus and neocortex), calretinin (CR) (neocortex), and VIP (neocortex), though none of these markers is specific for or ubiquitously expressed by CCK-expressing dendrite targeting interneurons.

    “Additional molecular markers commonly associated with hippocampal and neocortical CCK-expressing dendrite targeting interneurons are calbindin (CB) (hippocampus and neocortex), calretinin (CR) (neocortex), and VIP (neocortex), though none of these markers is specific for or ubiquitously expressed by CCK-expressing dendrite targeting interneurons (224, 556, 569, 584, 611, 612).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [224]

  • All CCK-expressing dendrite targeting cells dominantly target principal cell postsynaptic targets with ~6 synapses per connection.

    “All CCK-expressing dendrite targeting cells dominantly target principal cell postsynaptic targets with ~6 synapses per connection; however, a minority of terminals (~8%) innervate other interneurons (102, 224, 584, 1172).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [224]

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Authors
Cope, D. W., Maccaferri, G., Márton, L. F., Roberts, J. D. B., Cobden, P. M., & Somogyi, P.
Affiliations
University of Oxford (GB)
Corresponding author
Cope, D.W
ORCID
Venue
Neuroscience
Publisher
Elsevier BV
Published
2002-01
Volume
109
Issue
1
Pages
63-80
ISSN
0306-4522 (ISSN-L)
DOI
10.1016/s0306-4522(01)00440-7
OpenAlex
W2168534653
Cited by
144
References
118
Citations by year
2026: 3 · 2025: 5 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 2 · 2018: 7 · 2017: 5 · 2016: 7 · 2015: 4 · 2014: 4 · 2013: 7 · 2012: 6
FWCI
3.49
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords
basket cells, GABAergic interneurons, CA1 pyramidal neurons, dendritic innervation, calbindin, hippocampus development, stratum radiatum, membrane properties, postnatal development, rat hippocampus
MeSH terms
Action Potentials, Aging, Animals, Animals, Newborn, Axons, Cholecystokinin, gamma-Aminobutyric Acid, Hippocampus, Immunohistochemistry, Interneurons, Lysine, Male, Neural Inhibition, Synaptic Transmission, Organ Culture Techniques, Rats, Wistar, Pyramidal Cells, Rats, Calbindins, S100 Calcium Binding Protein G

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