The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
Parvalbumin Interneurons of Hippocampus Tune Population Activity at Theta Frequency
Open accessAbstract
Hippocampal theta rhythm arises from a combination of recently described intrinsic theta oscillators and inputs from multiple brain areas. Interneurons expressing the markers parvalbumin (PV) and somatostatin (SOM) are leading candidates to participate in intrinsic rhythm generation and principal cell (PC) coordination in distal CA1 and subiculum. We tested their involvement by optogenetically activating and silencing PV or SOM interneurons in an intact hippocampus preparation that preserves intrinsic connections and oscillates spontaneously at theta frequencies. Despite evidence suggesting that SOM interneurons are crucial for theta, optogenetic manipulation of these interneurons modestly influenced theta rhythm. However, SOM interneurons were able to strongly modulate temporoammonic inputs. In contrast, activation of PV interneurons powerfully controlled PC network and rhythm generation optimally at 8 Hz, while continuously silencing them disrupted theta. Our results thus demonstrate a pivotal role of PV but not SOM interneurons for PC synchronization and the emergence of intrinsic hippocampal theta.
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In the citing paper
“The frequency of theta oscillations can be experimentally manipulated by optogenetically activating pacemaker cells within the medial septum102 as well as local FS interneurons within the hippocampus103.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [103]
In the citing paper
“Optogenetic studies on the hippocampus have shown that parvalbumin (PV)+ interneurons are the main effectors of intrinsic theta rhythm”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [25]
In the citing paper
“while somatostatin (SST)+ interneurons modulate the entrainment of intrinsic theta by controlling external inputs to the hippocampus (25).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [25]
In the citing paper
“SST+ interneurons on the other hand have been demonstrated to indirectly contribute to the entrainment of theta oscillations in the hippocampus (25) and are responsible for preferentially driving beta (15–30 Hz) frequency oscillations in other brain regions (72).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [25]
In the citing paper
“GABAergic interneurons, especially the PV+ subtype, play an important role in the regulation of neuronal oscillations in the brain (24–27) and have also been implicated in neuropsychiatric disease (66; 67).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [25]
In the citing paper
“Therefore, the latter studies suggest an intrinsic ability of the CA1 circuit to generate some form of theta waves even without rhythmic external inputs.”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Amilhon et al., 2015
In the citing paper
“recent reports indicate the presence of spontaneous theta-frequency LFP oscillations even in the isolated whole CA1 preparation in vitro (Goutagny et al., 2009; Amilhon et al., 2015).”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Amilhon et al., 2015
In the citing paper
“Reassuringly, these results were in overall agreement with experimental data from the isolated CA1 preparation indicating that optogenetic silencing of PV+ cells, but not SOM+ cells such as the O-LM cells, caused a marked reduction in theta oscillations (Amilhon et al., 2015).”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Amilhon et al., 2015
In the citing paper
“Consistent with experimental results (Goutagny et al., 2009; Amilhon et al., 2015), these oscillations emerged from the network model without explicit encoding, rhythmic inputs or purposeful tuning of intra-CA1 parameters (all anatomical connectivity parameters were exactly as previously published in Bezaire and Soltesz (2013)).”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Amilhon et al., 2015
In the citing paper
“the experimental data on the isolated CA1 preparation were obtained from both rat (Goutagny et al., 2009) and mouse (Amilhon et al., 2015)”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Amilhon et al., 2015
Citations
Cites
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332
CircStat : A MATLAB Toolbox for Circular Statistics
Berens, P. (2009) · Journal of Statistical Software · doi:10.18637/jss.v031.i10 · Cited by 3,099
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050
Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons
Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., & Somogyi, P. (1995) · Nature · doi:10.1038/378075a0 · Cited by 1,498
GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus
Freund, T. F., & Antal, M. (1988) · Nature · doi:10.1038/336170a0 · Cited by 1,283
The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041
Chronux: A platform for analyzing neural signals
Bokil, H., Andrews, P., Kulkarni, J. E., Mehta, S. B., & Mitra, P. P. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.06.020 · Cited by 867
Adhikari, A., Topiwala, M. A., & Gordon, J. A. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.002 · Cited by 729
Amygdalar and Hippocampal Theta Rhythm Synchronization During Fear Memory Retrieval
Seidenbecher, T., Laxmi, T. R., Stork, O., & Pape, H.-C. (2003) · Science · doi:10.1126/science.1085818 · Cited by 728
Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition
Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., & Buzsáki, G. (2012) · Nature Neuroscience · doi:10.1038/nn.3077 · Cited by 728
Mechanisms and functions of theta rhythms
Colgin, L. L. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170330 · Cited by 559
Hippocampal theta oscillations are travelling waves
Lubenov, E. V., & Siapas, A. G. (2009) · Nature · doi:10.1038/nature08010 · Cited by 523
Dendritic Inhibition in the Hippocampus Supports Fear Learning
Lovett-Barron, M., Kaifosh, P., Kheirbek, M. A., Danielson, N., Zaremba, J. D., Reardon, T. R., Turi, G. F., Hen, R., Zemelman, B. V., & Losonczy, A. (2014) · Science · doi:10.1126/science.1247485 · Cited by 509
Maccaferri, G., & McBain, C. J. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021754 · Cited by 503
Han, X., Chow, B. Y., Zhou, H., Klapoetke, N. C., Chuong, A. S., Rajimehr, R., Yang, A., Baratta, M. V., Winkle, J. A., Desimone, R., et al. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2011.00018 · Cited by 490
High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels
Berndt, A., Schoenenberger, P., Mattis, J., Tye, K. M., Deisseroth, K. A., Hegemann, P., & Oertner, T. G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1017210108 · Cited by 442
Regulation of neuronal input transformations by tunable dendritic inhibition
Lovett-Barron, M., Turi, G. F., Kaifosh, P., Lee, P. H., Bolze, F., Sun, X.-H., Nicoud, J.-F., Zemelman, B. V., Sternson, S. M., & Losonczy, A. (2012) · Nature Neuroscience · doi:10.1038/nn.3024 · Cited by 417
Soltész, I., & Deschênes, M. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.97 · Cited by 410
Wulff, P., Ponomarenko, A. A., Bartos, M., Korotkova, T. M., Fuchs, E. C., Bähner, F., Both, M., Tort, A. B. L., Kopell, N. J., Wisden, W., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813176106 · Cited by 400
Ylinen, A., Soltész, I., Bragin, A., Penttonen, M., Attila Gabor, S. I. K., & Buzsáki, G. (1995) · Hippocampus · doi:10.1002/hipo.450050110 · Cited by 377
Pike, F. G., Goddard, R. S., Suckling, J. M., Ganter, P., Kasthuri, N., & Paulsen, O. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00205.x · Cited by 364
OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons
Leão, R. N., Mikulovic, S., Leão, K. E., Munguba, H., Gezelius, H., Enjin, A., Patra, K., Eriksson, A., Loew, L. M., Tort, A. B. L., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3235 · Cited by 359
Inhibition-induced theta resonance in cortical circuits
Stark, E., Eichler, R., Roux, L., Fujisawa, S., Rotstein, H. G., & Buzsáki, G. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.033 · Cited by 326
Traveling Theta Waves along the Entire Septotemporal Axis of the Hippocampus
Patel, J., Fujisawa, S., Berényi, A., Royer, S., & Buzsáki, G. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.015 · Cited by 302
Self-generated theta oscillations in the hippocampus
Goutagny, R., Jackson, J., & Williams, S. (2009) · Nature Neuroscience · doi:10.1038/nn.2440 · Cited by 301
Self-citationBehavior-dependent specialization of identified hippocampal interneurons
Lapray, D., Lasztóczi, B., Lagler, M., Viney, T. J., Katona, L., Valenti, O., Hartwich, K., Borhegyi, Z., Somogyi, P., & Klausberger, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3176 · Cited by 269
Varga, C., Golshani, P., & Soltesz, I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210929109 · Cited by 253
Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus
Gloveli, T., Dugladze, T., Rotstein, H. G., Traub, R. D., Monyer, H., Heinemann, U., Whittington, M. A., & Kopell, N. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506259102 · Cited by 234
Hippocampus, theta, and spatial memory
O'Keefe, J. M. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90163-s · Cited by 226
Interdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis
Kocsis, B., Bragin, A., & Buzsáki, G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-06200.1999 · Cited by 218
A Model of Atropine‐Resistant Theta Oscillations in Rat Hippocampal Area CA1
Gillies, M. J., Traub, R. D., LeBeau, F. E. N., Davies, C. H., Gloveli, T., Buhl, E., & Whittington, M. A. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.024588 · Cited by 203
Empson, R. M., & Heinemann, U. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020697 · Cited by 161
Fast and Slow Gamma Rhythms Are Intrinsically and Independently Generated in the Subiculum
Jackson, J., Goutagny, R., & Williams, S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1370-11.2011 · Cited by 108
Self-citationReversal of theta rhythm flow through intact hippocampal circuits
Jackson, J., Amilhon, B., Goutagny, R., Bott, J.-B., Manseau, F., Kortleven, C., Bressler, S. L., & Williams, S. (2014) · Nature Neuroscience · doi:10.1038/nn.3803 · Cited by 83
Self-citationSpike Resonance Properties in Hippocampal O-LM Cells Are Dependent on Refractory Dynamics
Kispersky, T. J., Fernandez, F. R., Economo, M. N., & White, J. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1361-11.2012 · Cited by 52
NMDA-Dependent Phase Synchronization between Septal and Temporal CA3 Hippocampal Networks
Gu, N., Jackson, J., Goutagny, R., Lowe, G. C., Manseau, F., & Williams, S. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0179-13.2013 · Cited by 17
Self-citationEpisodic memory, semantic memory, and amnesia
Squire, L. R., & Zola, S. M. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:3
Research works printed but not linked: 1
- Berens, 2009, CircStat: a MATLAB toolbox for circular statistics, J. Stat. Softw., 31, 1
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Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889
Oscillating circuitries in the sleeping brain
Adamantidis, A. R., Gutierrez Herrera, C., & Gent, T. C. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0223-4 · Cited by 281
Self-citationOptogenetic gamma stimulation rescues memory impairments in an Alzheimer’s disease mouse model
Etter, G., van der Veldt, S., Manseau, F., Zarrinkoub, I., Trillaud-Doppia, É., & Williams, S. (2019) · Nature Communications · doi:10.1038/s41467-019-13260-9 · Cited by 248
Self-citationOgnjanovski, N., Schaeffer, S. M., Wu, J., Mofakham, S., Maruyama, D., Żochowski, M., & Aton, S. J. (2017) · Nature Communications · doi:10.1038/ncomms15039 · Cited by 237
Functional neuronal circuitry and oscillatory dynamics in human brain organoids
Sharf, T., van der Molen, T., Glasauer, S. M. K., Guzman, E., Buccino, A. P., Luna, G., Cheng, Z., Audouard, M., Ranasinghe, K. G., Kudo, K., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32115-4 · Cited by 251
Metadata
- Authors
- Amilhon, B., Huh, C. Y. L., Manseau, F., Ducharme, G., Nichol, H., Adamantidis, A., & Williams, S.
- Affiliations
- Douglas Mental Health University Institute (CA)
- University of Bern (CH)
- Corresponding author
- Amilhon, Bénédicte
- Williams, Sylvain
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2015-06
- Volume
- 86
- Issue
- 5
- Pages
- 1277-1289
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W1544607115
- Cited by
- 241
- References
- 39
- Citations by year
- 2026: 13 · 2025: 24 · 2024: 16 · 2023: 28 · 2022: 26 · 2021: 22 · 2020: 27 · 2019: 22 · 2018: 24 · 2017: 24 · 2016: 13 · 2015: 2
- FWCI
- 12.62
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Massachusetts Institute of Technology
- McGill University
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- parvalbumin interneurons, somatostatin interneurons, hippocampal theta rhythm, optogenetic manipulation, CA1, subiculum, neural population activity
- MeSH terms
- Action Potentials, Animals, Animals, Newborn, Hippocampus, Interneurons, Organ Culture Techniques, Parvalbumins, Theta Rhythm, Mice
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