Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations

Klausberger, Thomas; Marton, Laszlo F.; O'Neill, Joseph; Huck, Jojanneke H. J.; Dalezios, Yannis; Fuentealba, Pablo; Suen, Wai Yee; Papp, Edit; Kaneko, Takeshi; Watanabe, Masahiko; Csicsvari, Jozsef; Somogyi, Peter

doi:10.1523/jneurosci.3269-05.2005

Cited by 469Neural dynamics and brain functionNeuroscience and Neuropharmacology ResearchMemory and Neural Mechanisms

Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations

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Klausberger, Thomas, Marton, Laszlo F., O'Neill, Joseph, Huck, Jojanneke H. J., Dalezios, Yannis, Fuentealba, Pablo, Suen, Wai Yee, Papp, Edit +4 more·2005·The Journal of Neuroscience

DOI 10.1523/jneurosci.3269-05.2005PMC PMC6725722

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Abstract

In the hippocampal CA1 area, a relatively homogenous population of pyramidal cells is accompanied by a diversity of GABAergic interneurons. Previously, we found that parvalbumin-expressing basket, axo-axonic, bistratified, and oriens-lacunosum moleculare cells, innervating different domains of pyramidal cells, have distinct firing patterns during network oscillations in vivo. A second family of interneurons, expressing cholecystokinin but not parvalbumin, is known to target the same domains of pyramidal cells as do the parvalbumin cells. To test the temporal activity of these independent and parallel GABAergic inputs, we recorded the precise spike timing of identified cholecystokinin interneurons during hippocampal network oscillations in anesthetized rats and determined their molecular expression profiles and synaptic targets. The cells were cannabinoid receptor type 1 immunopositive. Contrary to the stereotyped firing of parvalbumin interneurons, cholecystokinin-expressing basket and dendrite-innervating cells discharge, on average, with 1.7 +/- 2.0 Hz during high-frequency ripple oscillations in an episode-dependent manner. During theta oscillations, cholecystokinin-expressing interneurons fire with 8.8 +/- 3.3 Hz at a characteristic time on the ascending phase of theta waves (155 +/- 81 degrees), when place cells start firing in freely moving animals. The firing patterns of some interneurons recorded in drug-free behaving rats were similar to cholecystokinin cells in anesthetized animals. Our results demonstrate that cholecystokinin- and parvalbumin-expressing interneurons make different contributions to network oscillations and play distinct roles in different brain states. We suggest that the specific spike timing of cholecystokinin interneurons and their sensitivity to endocannabinoids might contribute to differentiate subgroups of pyramidal cells forming neuronal assemblies, whereas parvalbumin interneurons contribute to synchronizing the entire network.

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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 [584]
ADIs are similar to SCAs but preferentially innervate the main apical shaft of pyramidal cells avoiding oblique and basal dendrites.
“Apical dendrite targeting interneurons (ADIs) are similar to SCAs but preferentially innervate the main apical shaft of pyramidal cells avoiding oblique and basal dendrites (584).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [584]
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 [584]
The axons of PPAs concentrate within s.l.m. overlapping with excitatory inputs from the entorhinal cortex and nucleus reuniens targeting the distal apical tufts of CA1 pyramidal cells.
“The axons of perforant path-associated cells (PPAs) concentrate within s.l.m. overlapping with excitatory inputs from the entorhinal cortex and nucleus reuniens targeting the distal apical tufts of CA1 pyramidal cells (584, 1172).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [584]
PPAs also extend axon collaterals across the hippocampal fissure to target the dendrites of granule cells further aligning their output with excitatory entorhinal input to the hippocampus.
“However, PPAs also extend axon collaterals across the hippocampal fissure to target the dendrites of granule cells further aligning their output with excitatory entorhinal input to the hippocampus (452, 584, 1172).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [584]

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 [584]
CCK-expressing dendrite targeting interneurons generally extend multipolar dendrites spanning all layers, though horizontally oriented dendritic arbors mostly confined to s.r. have also been observed.
“They generally extend multipolar dendrites spanning all layers, though horizontally oriented dendritic arbors mostly confined to s.r. have also been observed (181, 224, 452, 584, 654, 885, 1172).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [584]
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 [584]
Like CCKBCs, dendrite targeting CCK interneuron subtypes typically express CB1Rs.
“Like CCKBCs, dendrite targeting CCK interneuron subtypes typically express CB1Rs (FIGURE 3B) (108, 289, 584, 594, 665, 1194).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [584]
VGluT3 expression was originally described as being limited to CCKBCs, it has also been detected in ADIs.
“While VGluT3 expression was originally described as being limited to CCKBCs (1031), it has also been detected in ADIs (584).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [584]
Cells in cluster 6 had the highest incidence of CCK expression (typically in combination with VGluT3 and VIP) and anatomies indicative of CCKBCs and mossy fiber associated cells, with intrinsic features often intermediate to cells in all other clusters.
“Finally, cells in cluster 6 had the highest incidence of CCK expression (typically in combination with VGluT3 and VIP) and anatomies indicative of CCKBCs (1031, 584) and mossy fiber associated cells (1138) with intrinsic features that were often intermediate to cells in all other clusters (TABLE 1).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [584]
Distinct interneuronal types exhibit characteristic, cell-type-specific preferred phases of firing during theta oscillations in vivo.
“As mentioned above, distinct interneuronal types, defined based on their selective axonal innervation patterns of the postsynaptic domains of pyramidal cells, exhibit characteristic, cell-type-specific preferred phases of firing during theta oscillations in vivo (Klausberger et al., 2003; 2004, 2005; Ferraguti et al., 2005; Jinno et al., 2007; Fuentealba et al., 2008; Varga et al., 2012; Lapray et”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Klausberger et al., 2005

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Authors: Klausberger, T., Marton, L. F., O'Neill, J., Huck, J. H. J., Dalezios, Y., Fuentealba, P., Suen, W. Y., Papp, E., Kaneko, T., Watanabe, M., Csicsvari, J., & Somogyi, P.
Affiliations: University of Oxford (GB)
Kyoto University (JP)
Hokkaido University (JP)
ORCID: Klausberger, Thomas
Huck, Jojanneke H. J.
Dalezios, Yannis
Fuentealba, Pablo
Papp, Edit
Kaneko, Takeshi
Watanabe, Masahiko
Csicsvari, Jozsef
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2005-10-19
Volume: 25
Issue: 42
Pages: 9782-9793
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.3269-05.2005
PMC: PMC6725722
OpenAlex: W2103322364
Cited by: 469
References: 76
Citations by year: 2026: 16 · 2025: 26 · 2024: 17 · 2023: 20 · 2022: 17 · 2021: 20 · 2020: 23 · 2019: 15 · 2018: 27 · 2017: 19 · 2016: 25 · 2015: 24 · 2014: 28 · 2013: 19 · 2012: 19
FWCI: 9.23
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 182 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
Funders: Austrian Science Fund (P16637)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: cholecystokinin interneurons, parvalbumin interneurons, GABAergic interneurons, hippocampal CA1, theta oscillations, ripple oscillations, basket cells, axo-axonic cells, spike timing, endocannabinoids, cannabinoid receptor type 1, cell assemblies, pyramidal neurons
MeSH terms: Action Potentials, Animals, Biological Clocks, Cholecystokinin, gamma-Aminobutyric Acid, Gene Expression Regulation, Hippocampus, Male, Nerve Net, Neurons, Parvalbumins, Rats, Sprague-Dawley, Receptors, GABA, Rats

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Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations

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