Chronometric readout from a memory trace: Gamma-frequency field stimulation recruits timed recurrent activity in the rat CA3 network
Abstract
Synchronous population activity is prevalent in neurones of the central nervous system and experimentally captured as oscillatory electric fields, the frequency of which can represent the state of the neural circuit, e.g. theta (approximately 5 Hz) and gamma (approximately 40 Hz). Such field oscillations, however, are not merely a result of coherent neuronal activity. They may also play active roles in information processing in the brain. In this study, we observed that, in cultured hippocampal slices, CA3 pyramidal cells responded to single-pulse stimuli with monosynaptic and polysynaptic potentials and firing spikes which occurred after variable latencies. The variability of the spike latencies was greatly reduced in the presence of weak electric field oscillations, especially the oscillation in the gamma-band frequency range, that per se induced only small fluctuations in the subthreshold membrane potential, and this effect was inhibited by blockade of NMDA receptor activity. Furthermore, the latency of the firing spikes changed if the stimulus was applied at a different phase of the imposed gamma oscillations. These results may suggest that the background field oscillations serve as an extracellular time reference and assure accurate and stable decoding of a memory trace present in cortical feedback networks.
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External oscillating electric fields modulate the firing pattern of individual neurons in rat hippocampal slices.
“Clearly the external fields were modulating the firing pattern of individual neurons.”
From The electromagnetic will (2021) · cites this paper as [67]
Cites
The brainweb: phase synchronization and large-scale integration
Varela, F., Lachaux, J.-P., Rodriguez, E., & Martinerie, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35067550 · Cited by 4,761 · see citing works
Bi, G.-Q., & Poo, M.-M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10464.1998 · Cited by 4,744 · see citing works
Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs
Markram, H., Lübke, J., Frotscher, M., & Sakmann, B. (1997) · Science · doi:10.1126/science.275.5297.213 · Cited by 3,832 · see citing works
Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention
Fries, P., Reynolds, J. H., Rorie, A. E., & Desimone, R. (2001) · Science · doi:10.1126/science.1055465 · Cited by 2,786 · see citing works
Neuronal Synchrony: A Versatile Code for the Definition of Relations?
Singer, W. (1999) · Neuron · doi:10.1016/s0896-6273(00)80821-1 · Cited by 2,581 · see citing works
Koch, C. (1998) · Oxford University Press eBooks · doi:10.1093/oso/9780195104912.001.0001 · Cited by 2,306 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat
Bragin, A., Jando, G., Nadasdy, Z., Hetke, J., Wise, K., & Buzsaki, G. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00047.1995 · Cited by 1,527 · see citing works
The high-conductance state of neocortical neurons in vivo
Alain Destexhe, A., Rudolph, M., & Paré, D. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1198 · Cited by 1,077 · see citing works
Synaptic reverberation underlying mnemonic persistent activity
Wang, X.-J. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01868-3 · Cited by 1,059 · see citing works
Synchronous neural oscillations and cognitive processes
Ward, L. M. (2003) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2003.10.012 · Cited by 1,009 · see citing works
Stable propagation of synchronous spiking in cortical neural networks
Diesmann, M., Gewaltig, M.-O., & Aertsen, A. (1999) · Nature · doi:10.1038/990101 · Cited by 1,003 · see citing works
Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat
Csicsvari, J., Jamieson, B. G., Wise, K. D., & Buzsáki, G. (2003) · Neuron · doi:10.1016/s0896-6273(02)01169-8 · Cited by 990 · see citing works
Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro
Fisahn, A., Pike, F. G., Buhl, E. H., & Paulsen, O. (1998) · Nature · doi:10.1038/28179 · Cited by 884 · see citing works
Organization of cell assemblies in the hippocampus
Harris, K. D., Csicsvari, J., Hirase, H., Dragoi, G., & Buzsáki, G. (2003) · Nature · doi:10.1038/nature01834 · Cited by 869 · see citing works
Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory
Wang, X.-J. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09587.1999 · Cited by 859 · see citing works
Synchronous oscillations in neuronal systems: Mechanisms and functions
Gray, C. M. (1994) · Journal of Computational Neuroscience · doi:10.1007/bf00962716 · Cited by 787 · see citing works
Graded persistent activity in entorhinal cortex neurons
Egorov, A. V., Hamam, B. N., Fransén, E., Hasselmo, M. E., & Alonso, A. A. (2002) · Nature · doi:10.1038/nature01171 · Cited by 769 · see citing works
Neurocomputational models of working memory
Durstewitz, D., Seamans, J. K., & B, T. J. S. A. (2000) · Nature Neuroscience · doi:10.1038/81460 · Cited by 710 · see citing works
Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling
Fell, J., Klaver, P., Lehnertz, K., Grünwald, T., Schaller, C., Elger, C. E., & Fernández, G. (2001) · Nature Neuroscience · doi:10.1038/nn759 · Cited by 692 · see citing works
Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions
Jefferys, J. G. R. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.4.689 · Cited by 686 · see citing works
Dopamine-Mediated Stabilization of Delay-Period Activity in a Network Model of Prefrontal Cortex
Durstewitz, D., Seamans, J. K., & B, T. J. S. A. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.3.1733 · Cited by 617 · see citing works
A role for NMDA-receptor channels in working memory
Lisman, J. E., Fellous, J., & Wang, X. (1998) · Nature Neuroscience · doi:10.1038/1086 · Cited by 438 · see citing works
Single neurones can initiate synchronized population discharge in the hippocampus
Miles, R., & Wong, R. K. S. (1983) · Nature · doi:10.1038/306371a0 · Cited by 403 · see citing works
Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons
Shu, Y., Hasenstaub, A., Badoual, M., Bal, T., & McCormick, D. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10388.2003 · Cited by 298 · see citing works
Memory from the dynamics of intrinsic membrane currents
Marder, E., Abbott, L. F., Turrigiano, G. G., Liu, Z., & Golowasch, J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13481 · Cited by 281 · see citing works
Dynamics of a recurrent network of spiking neurons before and following learning
Amit, D. J., & Brunel, N. (1997) · Network Computation in Neural Systems · doi:10.1088/0954-898x_8_4_003 · Cited by 241 · see citing works
Cholinergic modulation of the cortical neuronal network
Lucas-Meunier, E., Fossier, P., Baux, G., & Amar, M. (2003) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-002-0999-2 · Cited by 207 · see citing works
Simple Networks for Spike-Timing-Based Computation, with Application to Olfactory Processing
Brody, C. D., & Hopfield, J. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00120-x · Cited by 192 · see citing works
de Toledo‐Morrell, L., Dickerson, B. C., Sullivan, M. P. O., Spanovic, C., Wilson, R. S., & Bennett, D. A. (2000) · Hippocampus · doi:10.1002/(sici)1098-1063(2000)10:2 · Cited by 178 · see citing works
Space-Clamp Problems When Voltage Clamping Branched Neurons With Intracellular Microelectrodes
Rall, W., & Segev, I. (1985) · Springer eBooks · doi:10.1007/978-1-4614-7601-6_9 · Cited by 100 · see citing works
Interplay of Electroencephalogram Phase and Auditory-Evoked Neural Activity
Kruglikov, S. Y., & Schiff, S. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-10122.2003 · Cited by 85 · see citing works
Timing of neural responses in cortical organotypic slices
Buonomano, D. V. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0736909100 · Cited by 83 · see citing works
Ikegaya, Y. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-02-00802.1999 · Cited by 53 · see citing works
Self-citationMemory: Recording experience in cells and circuits: Diversity in memory research
Goldman, P. S. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13435 · Cited by 41 · see citing works
BDNF Boosts Spike Fidelity in Chaotic Neural Oscillations
Fujisawa, S., Yamada, M. K., Nishiyama, N., Matsuki, N., & Ikegaya, Y. (2004) · Biophysical Journal · doi:10.1016/s0006-3495(04)74249-6 · Cited by 26 · see citing works
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Fröhlich, F., & McCormick, D. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.005 · Cited by 913 · see citing works
Ephaptic coupling to endogenous electric field activity: Why bother?
Anastassiou, C. A., & Koch, C. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.09.002 · Cited by 171 · see citing works
Integrating information in the brain's EM field: the cemi field theory of consciousness
McFadden, J. (2020) · Neuroscience of Consciousness · doi:10.1093/nc/niaa016 · Cited by 148 · see citing works
McFadden, J. (2021) · NeuroSci · doi:10.3390/neurosci2030021 · Cited by 13 · see citing works
- Authors
- Fujisawa, S., Matsuki, N., & Ikegaya, Y.
- Affiliations
- The University of Tokyo (JP)
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2004-11
- Volume
- 561
- Issue
- 1
- Pages
- 123-131
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- OpenAlex
- W2142063073
- Cited by
- 36
- References
- 36
- Citations by year
- 2025: 5 · 2023: 1 · 2021: 1 · 2020: 2 · 2015: 1 · 2014: 3 · 2013: 4 · 2012: 2
- FWCI
- 1.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- 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
- gamma oscillations, hippocampal CA3, field oscillations, spike latency, NMDA receptor, memory traces, hippocampal slices
- MeSH terms
- Action Potentials, Animals, Association Learning, Electric Stimulation, Hippocampus, Memory, Short-Term, Organ Culture Techniques, Periodicity, Reaction Time, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Rats
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