Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition
Open accessAbstract
A consortium of inhibitory neurons control the firing patterns of pyramidal cells, but their specific roles in the behaving animal are largely unknown. We performed simultaneous physiological recordings and optogenetic silencing of either perisomatic (parvalbumin (PV) expressing) or dendrite-targeting (somatostatin (SOM) expressing) interneurons in hippocampal area CA1 of head-fixed mice actively moving a treadmill belt rich with visual-tactile stimuli. Silencing of either PV or SOM interneurons increased the firing rates of pyramidal cells selectively in their place fields, with PV and SOM interneurons having their largest effect during the rising and decaying parts of the place field, respectively. SOM interneuron silencing powerfully increased burst firing without altering the theta phase of spikes. In contrast, PV interneuron silencing had no effect on burst firing, but instead shifted the spikes' theta phase toward the trough of theta. These findings indicate that perisomatic and dendritic inhibition have distinct roles in controlling the rate, burst and timing of hippocampal pyramidal cells.
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Interneurons targeting the perisomatic area of pyramidal cells, such as PV, CCK basket, and chandelier cells, more strongly regulate spike output, timing, and population firing synchrony.
“In contrast INs that target the perisomatic area of PCs, such as PV and CCK basket cells and chandelier cells have a stronger influence on regulating the spiking output of the cell, its timing and thus the firing synchrony of populations of neurons (Cobb et al., 1995; Miles et al., 1996; Royer et al., 2012).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Royer et al., 2012
The Results section (“Control of spike theta phase by somatic inhibition”; page unavailable) finds that PV-mediated perisomatic inhibition regulates spike timing more strongly than dendritic inhibition. It does not establish stronger control of firing rate—the two manipulations produced similar rate increases—and the cited findings do not establish population synchrony or the effects of CCK basket and chandelier cells. (LLM, conf=0.88)
Experimental — accuracy not yet measuredRunning along the treadmill reliably engaged the hippocampal place representation, with 340 out of 520 putative principal neurons classified as place cells.
“Consistent with previous work37–39, running along the treadmill reliably engaged the hippocampal place representation, with the large majority of putative principal neurons (340 out of 520) being classified as place cells (see Methods).”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [37]
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- Authors
- Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., & Buzsáki, G.
- Affiliations
- Howard Hughes Medical Institute (US)
- Rutgers, The State University of New Jersey (US)
- Corresponding author
- Magee, Jeffrey C
- Buzsáki, György
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2012-03-25
- Volume
- 15
- Issue
- 5
- Pages
- 769-775
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4919905
- OpenAlex
- W2061960110
- Cited by
- 728
- References
- 58
- Citations by year
- 2026: 35 · 2025: 61 · 2024: 52 · 2023: 60 · 2022: 53 · 2021: 55 · 2020: 55 · 2019: 60 · 2018: 47 · 2017: 42 · 2016: 45 · 2015: 43 · 2014: 62 · 2013: 41 · 2012: 17
- FWCI
- 26.67
- Type
- journal article
- Language
- en
- Update notices
- erratum (2013-11-22)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (R01MH054671, MH54671)
- National Institute of Neurological Disorders and Stroke (R01NS034994, NS-34994)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- place cells, parvalbumin interneurons, somatostatin interneurons, dendritic inhibition, perisomatic inhibition, burst firing, spike timing, theta phase, CA1, optogenetic silencing, place fields
- MeSH terms
- Action Potentials, Animals, Behavior, Animal, Biophysics, Dendrites, Electric Stimulation, Exercise Test, Hippocampus, Humans, Light, Mice, Inbred C57BL, Mice, Transgenic, Movement, Neural Inhibition, Neurons, Parvalbumins, Photic Stimulation, Probability, Somatostatin, Spectrum Analysis, Time Factors, Time Perception, Touch, Patch-Clamp Techniques, Halorhodopsins, Green Fluorescent Proteins, Mice, Optics and Photonics
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