Abstract
In this chapter we shall begin consideration of one of the prevailing hypotheses concerning the function of network oscillations in the brain: that oscillations are used for communication between spatially separated groups of neurons (Wilson et al., F1000Res 7:F1000 Faculty Rev-1960, 2018; Cannon et al., Eur J Neurosci 39:705–719, 2014). Cannon et al. (Eur J Neurosci 39:705–719, 2014) emphasize – correctly, we believe – that proper understanding of oscillatory communication requires detailed analysis of the underlying cellular mechanisms, rather than just describing the frequency or the areas involved. Besides mechanisms, one must additionally understand, however, just what it is that is to be communicated. Here again, we shall pursue a prevailing hypothesis that it is the contents of cell assemblies, that is, the identities of the constituent cells – which one network needs to convey to another network. That is the underlying function, so we believe, of most of the forebrain.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Cannon J, McCarthy MM, Lee S, Lee J, Börgers C, Whittington MA, Kopell N (2014) Neurosystems: brain rhythms and cognitive processing. Eur J Neurosci 39:705–719
Charpak S, Gähwiler BJ, Do KQ, Knöpfel T (1990) Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature 347:765–767
Choi GB, Stettler DD, Kallman BR, Bhaskar ST, Fleischmann A, Axel R (2011) Driving opposing behaviors with ensembles of piriform neurons. Cell 146:1004–1015
Colling SB, Stanford IM, Traub RD, Jefferys JGR (1998) Limbic gamma rhythms. I. Phase-locked oscillations in hippocampal CA1 and subiculum. J Neurophysiol 80:155–161
Deuchars J, Thomson AM (1996) CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74:1009–1018
Dugladze T, Schmitz D, Whittington MA, Vida I, Gloveli T (2017) Segregation of axonal and somatic activity during fast network oscillations. Science 336:1458–1461
Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ (1988) Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol Cybern 60:121–130
Eliav T, Geva-Sagiv M, Yartsev MM, Finkelstein A, Rubin A, Las L, Ulanovsky N (2018) Nonoscillatory phase coding and synchronization in the bat hippocampal formation. Cell 175:1119–1130.e15
Engel AK, König P, Gray CM, Singer W (1990) Stimulus-dependent neuronal oscillations in cat visual cortex: inter-columnar interaction as determined by cross-correlation analysis. Eur J Neurosci 2:588–606
Ermentrout GB, Kopell N (1998) Fine structure of neural spiking and synchronization in the presence of conduction delays. Proc Natl Acad Sci USA 95:1259–1264
Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186–189
Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224
Fries P (2015) Rhythms for cognition: communication through coherence. Neuron 88:220–235
Fuchs EC, Doheny H, Faulkner H, Caputi A, Traub RD, Bibbig A, Kopell N, Whittington MA, Monyer H (2001) Genetically altered AMPA-type glutamate receptor kinetics in interneurons disrupt long-range synchrony of gamma oscillation. Proc Natl Acad Sci USA 98:3571–3576
Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, LeBeau FEN, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JNP, Monyer H (2007) Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53:591–604
Galambos R, Makeig S, Talmachoff PJ (1981) A 40-Hz auditory potential recorded from the human scalp. Proc Natl Acad Sci USA 78:2643–2647
Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86:1698–1702
Gray CM, König P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337
Guérineau NC, Gähwiler BH, Gerber U (1994) Reduction of resting K+ current by metabotropic glutamate and muscarinic receptors in rat CA3 cells: mediation by G-proteins. J Physiol 474:27–33
Harvey M, Lau D, Civillico E, Rudy B, Contreras D (2012) Impaired long-range synchronization of gamma oscillations in the neocortex of a mouse lacking Kv3.2 potassium channels. J Neurophysiol 108:827–833
Isomura Y, Sirota A, Ozen S, Montgomery S, Mizuseki K, Henze DA, Buzáki G (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52:871–882
Jagadeesh B, Gray CM, Ferster D (1992) Visually evoked oscillations of membrane potential in cells of cat visual cortex. Science 257:552–554
Kane L, Venniro M, Quintana-Feliciano R, Madangopal R, Rubio FJ, Bosseret JM, Caprioli D, Shaham Y, Hope BT, Warren BL (2021) Fos-expressing neuronal ensemble in rat ventromedial prefrontal cortex encodes cocaine seeking but not food seeking in rats. Addict Biol 26:e12943
Klein AS, Donoso JR, Kempter R, Schmitz D, Beed P (2016) Early cortical changes in gamma oscillations in Alzheimer’s disease. Front Syst Neurosci 10:83
Kopell N, Ermentrout GB, Whittington MA, Traub RD (2000) Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci USA 97:1867–1872
Kopell N, Kramer MA, Malerba P, Whittington MA (2010) Are different rhythms good for different functions? Front Hum Neurosci 4:187. https://doi.org/10.3389/fnhum.2010.00187
Maier N, Nimmrich V, Draguhn A (2003) Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550:873–887
Meissner-Bernard C, Dembitskaya Y, Venance L, Fleischmann A (2019) Encoding of odor-fear memories in the mouse olfactory cortex. Curr Biol 29:367–380.e4
Miles R, Wong RKS (1987) Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol 388:611–629
Nakazono T, Lam TN, Patel AY, Kitazawa M, Saito T, Saido TC, Igarashi KM (2017) Impaired in vivo gamma oscillations in the medial entorhinal cortex of knock-in Alzheimer model. Front Syst Neurosci 11:48
Nakazono T, Jun H, Blurton-Jones M, Green KN, Igarashi KM (2018) Gamma oscillations in the entorhinal-hippocampal circuit underlying memory and dementia. Neurosci Res 129:40–46
Nimmrich V, Maier N, Schmitz D, Draguhn A (2005) Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. J Physiol 563:663–670
Palm G (1982) Neural assemblies. Springer, Berlin
Papadimitriou CH, Vempala SS, Mitropolsky D, Collins M, Maass W (2020) Brain computation by assemblies of neurons. Proc Natl Acad Sci USA 117:14464–14472
Redondo RL, Kim J, Arons AL, Ramirez S, Liu X, Tonegawa S (2014) Bidirectional switch of the valence associated with a hippocampal contextual memory engram. Nature 513:426–430
Roelfsema PR, König P, Engel AK, Sireteanu R, Singer W (1994) Reduced synchronization in the visual cortex of cats with strabismic amblyopia. Eur J Neurosci 6:1645–1655
Sierra RO, Pedraza LK, Barcsai L, Pe** A, Li Q, Kozák G, Takeuchi Y, Nagy AJ, Lörincz ML, Devinsky O, Buzáki G, Berényi A (2023) Closed-loop brain stimulation augments fear extinction in male rats. Nat Commun 14:3972
Singer W (2021) Recurrent dynamics in the cerebral cortex: integration of sensory evidence with stored knowledge. Proc Natl Acad Sci USA 118:e2101043118
Symanski CA, Bladon JH, Kullberg ET, Miller P, Jadhav SP (2022) Rhythmic coordination and ensemble dynamics in the hippocampal-prefrontal network during odor-place associative memory and decision making. elife 11:e79545
Takatoh J, Prevosto V, Thompson PM, Lu J, Chung L, Harrahill A, Li S, Zhao S, He Z, Golomb D, Kleinfeld D, Wang F (2022) The whisking oscillator circuit. Nature 609:560–568
Traub RD, Miles R (1991) Neuronal networks of the hippocampus. Cambridge University Press, New York
Traub RD, Whittington MA (2010) Cortical oscillations in health and disease. Oxford University Press, New York
Traub RD, Borck C, Colling SB, Jefferys JGR (1996a) On the structure of ictal events in vitro. Epilepsia 37:879–891
Traub RD, Whittington MA, Stanford IM, Jefferys JGR (1996b) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:621–624
Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JGR (1996c) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 493:471–484
Traub RD, Jefferys JGR, Whittington MA (1997) Simulation of gamma rhythms in networks of interneurons and pyramidal cells. J Comput Neurosci 4:141–150
Traub RD, Whittington MA, Buhl EH, Jefferys JGR, Faulkner HJ (1999b) On the mechanism of the γ➔β frequency shift in neuronal oscillations induced in rat hippocampal slices by tetanic stimulation. J Neurosci 19:1088–1105
Traub RD, Jefferys JGR, Whittington MA (1999c) Fast oscillations in cortical circuits. MIT Press, Cambridge, MA
Traub RD, Bibbig A, Fisahn A, LeBeau FEN, Whittington MA, Buhl EH (2000) A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur J Neurosci 12:4093–4106
Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FEN, Whittington MA (2001c) Gap junctions between interneuron dendrites can enhance long-range synchrony of gamma oscillations. J Neurosci 21:9478–9486
Traub RD, Tu Y, Whittington MA (2021) Cell assembly formation and structure in a piriform cortex model. Rev Neurosci 33:111–132
Trimper JB, Colgin LL (2018) Spike time synchrony in the absence of continuous oscillations. Neuron 100:527–529
von der Malsburg C (1995) Binding in models of perception and brain function. Curr Opin Neurobiol 5:520–526
von der Malsburg C (2021) Toward understanding the neural code of the brain. Biol Cybern 115:439–449
von Stein A, Rappelsberger P, Sarnthein J, Petsche H (1999) Synchronization between temporal and parietal cortex during multimodal object processing in man. Cereb Cortex 9:137–150
Welsh JP, Llinás R (1997) Some organizing principles for the control of movement based on olivocerebellar physiology. Prog Brain Res 114:449–461
Whittington MA, Traub RD, Jefferys JGR (1995a) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612–615
Whittington MA, Stanford IM, Colling SB, Jefferys JGR, Traub RD (1997a) Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol 502:591–607
Whittington MA, Traub RD, Faulkner HJ, Stanford IM, Jefferys JG (1997b) Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscillations. Proc Natl Acad Sci USA 94:12198–12203
Wilson CJ, Higgs MH, Simmons DV, Morales JC (2018) Oscillations and spike entrainment. F1000Res 7:F1000 Faculty Rev-1960
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Traub, R., Draguhn, A. (2024). Oscillation Synchronization, Synaptic Plasticity, and Cell Assemblies. In: Brain Leitmotifs. Springer, Cham. https://doi.org/10.1007/978-3-031-54537-5_10
Download citation
DOI: https://doi.org/10.1007/978-3-031-54537-5_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-54536-8
Online ISBN: 978-3-031-54537-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)