Defined types of cortical interneurone structure space and spike timing in the hippocampus
Abstract
The cerebral cortex encodes, stores and combines information about the internal and external environment in rhythmic activity of multiple frequency ranges. Neurones of the cortex can be defined, recognized and compared on the comprehensive application of the following measures: (i) brain area- and cell domain-specific distribution of input and output synapses, (ii) expression of molecules involved in cell signalling, (iii) membrane and synaptic properties reflecting the expression of membrane proteins, (iv) temporal structure of firing in vivo, resulting from (i)-(iii). Spatial and temporal measures of neurones in the network reflect an indivisible unity of evolutionary design, i.e. neurones do not have separate structure or function. The blueprint of this design is most easily accessible in the CA1 area of the hippocampus, where a relatively uniform population of pyramidal cells and their inputs follow an instantly recognizable laminated pattern and act within stereotyped network activity patterns. Reviewing the cell types and their spatio-temporal interactions, we suggest that CA1 pyramidal cells are supported by at least 16 distinct types of GABAergic neurone. During a given behaviour-contingent network oscillation, interneurones of a given type exhibit similar firing patterns. During different network oscillations representing two distinct brain states, interneurones of the same class show different firing patterns modulating their postsynaptic target-domain in a brain-state-dependent manner. These results suggest roles for specific interneurone types in structuring the activity of pyramidal cells via their respective target domains, and accurately timing and synchronizing pyramidal cell discharge, rather than providing generalized inhibition. Finally, interneurones belonging to different classes may fire preferentially at distinct time points during a given oscillation. As different interneurones innervate distinct domains of the pyramidal cells, the different compartments will receive GABAergic input differentiated in time. Such a dynamic, spatio-temporal, GABAergic control, which evolves distinct patterns during different brain states, is ideally suited to regulating the input integration of individual pyramidal cells contributing to the formation of cell assemblies and representations in the hippocampus and, probably, throughout the cerebral cortex.
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In hippocampal CA1, an interneuron classification starting with morphological features has been successfully implemented.
“In the hippocampal CA1 region, Somogyi and his colleagues have been successful at implementing an interneuron classification that starts with morphological features, i.e. somatic location and dendritic and axonal innervation fields”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Somogyi and Klausberger, 2005
Inhibitory interneurons regulate network oscillations, which synchronize neuronal activity to rhythms that are crucial to learning and memory.
“Inhibitory interneurons regulate network oscillations, which synchronize neuronal activity to rhythms that are crucial to learning and memory [112–116].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [114]
Anatomical specialization among cortical interneuron subtypes allows for a division of labor that affords inhibitory networks spatiotemporal control over principal cell activity, rather than providing generalized inhibition.
“Indeed, it is now recognized that anatomical specialization among cortical interneuron subtypes allows for a division of labor that affords inhibitory networks exquisite spatiotemporal control over principal cell activity, rather than providing generalized inhibition (586, 1036).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1036]
CCK-expressing dendrite targeting interneurons together comprise between 3 and 5% (~1,500 cells) of CA1 interneurons (~0.4% of all CA1 neurons).
“CCK-expressing dendrite targeting interneurons together comprise between 3 and 5% (~1,500 cells) of CA1 interneurons (~0.4% of all CA1 neurons), largely reside in s.r., with some tendency to concentrate at the s.r./s.l.m. border.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1036]
CCK expression can be detected in a variety of dendrite targeting inhibitory interneurons that largely parse on the basis of axon termination zones across distinct pyramidal cell dendritic compartments.
“In addition to CCKBCs, CCK expression can also be detected in a variety of dendrite targeting inhibitory interneurons that largely parse on the basis of axon termination zones across distinct pyramidal cell dendritic compartments (102, 581, 1036).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1036]
CCK-expressing dendrite targeting interneurons largely reside in s.r., with some tendency to concentrate at the s.r./s.l.m. border.
“CCK-expressing dendrite targeting interneurons together comprise between 3 and 5% (~1,500 cells) of CA1 interneurons (~0.4% of all CA1 neurons), largely reside in s.r., with some tendency to concentrate at the s.r./s.l.m. border.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1036]
Local circuit interneuron axons possess considerable diversity in the targeting of their downstream postsynaptic domains.
“As described in section II, local circuit interneuron axons possess considerable diversity in the targeting of their downstream postsynaptic domains (352, 582, 1036) (FIGURE 1).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1036]
Rigorous and quantitative definitions of a neuron type have remained elusive.
“The notion of a ‘neuron type’, with similar properties among its members, as the basic unit of brain circuits has been an important concept for over a century; however, rigorous and quantitative definitions have remained surprisingly elusive1–5.”
From A multimodal cell census and atlas of the mammalian primary motor cortex (2021) · cites this paper as [1]
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- Authors
- Somogyi, P., & Klausberger, T.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Klausberger, Thomas
- ORCID
- Klausberger, Thomas
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2004-12-22
- Volume
- 562
- Issue
- 1
- Pages
- 9-26
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- OpenAlex
- W2114502694
- Cited by
- 927
- References
- 15
- Citations by year
- 2026: 10 · 2025: 23 · 2024: 20 · 2023: 20 · 2022: 20 · 2021: 30 · 2020: 24 · 2019: 38 · 2018: 42 · 2017: 37 · 2016: 41 · 2015: 43 · 2014: 49 · 2013: 61 · 2012: 57
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Oxford
- Austrian Science Fund
- Institute of Materials Research and Engineering
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- hippocampal CA1, cortical interneurons, pyramidal neurons, spike timing, network oscillations, brain states, cell assemblies, cerebral cortex
- MeSH terms
- Animals, Brain, Cerebral Cortex, Electrophysiology, Hippocampus, Humans, Interneurons, Neurons, Theta Rhythm
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