Theta-paced flickering between place-cell maps in the hippocampus: A model based on short-term synaptic plasticity
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
28558154
PubMed Central
PMC5575492
DOI
10.1002/hipo.22743
Knihovny.cz E-zdroje
- Klíčová slova
- CA3, attractor neural network, hippocampus, memory, place cell, recurrent neural network, teleportation, theta,
- MeSH
- akční potenciály fyziologie MeSH
- časové faktory MeSH
- elektroencefalografie MeSH
- hipokampus cytologie MeSH
- krysa rodu Rattus MeSH
- mapování mozku MeSH
- modely neurologické * MeSH
- nervová síť fyziologie MeSH
- neurony fyziologie MeSH
- neuroplasticita fyziologie MeSH
- podněty MeSH
- prostorová paměť fyziologie MeSH
- světelná stimulace MeSH
- theta rytmus EEG fyziologie MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Hippocampal place cells represent different environments with distinct neural activity patterns. Following an abrupt switch between two familiar configurations of visual cues defining two environments, the hippocampal neural activity pattern switches almost immediately to the corresponding representation. Surprisingly, during a transient period following the switch to the new environment, occasional fast transitions between the two activity patterns (flickering) were observed (Jezek, Henriksen, Treves, Moser, & Moser, ). Here we show that an attractor neural network model of place cells with connections endowed with short-term synaptic plasticity can account for this phenomenon. A memory trace of the recent history of network activity is maintained in the state of the synapses, allowing the network to temporarily reactivate the representation of the previous environment in the absence of the corresponding sensory cues. The model predicts that the number of flickering events depends on the amplitude of the ongoing theta rhythm and the distance between the current position of the animal and its position at the time of cue switching. We test these predictions with new analysis of experimental data. These results suggest a potential role of short-term synaptic plasticity in recruiting the activity of different cell assemblies and in shaping hippocampal activity of behaving animals.
Biomedical Center Faculty of Medicine in Pilsen Charles University Pilsen 32300 Czech Republic
Department of Neurobiology Weizmann Institute of Science Rehovot 76100 Israel
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Battaglia, F. P. , & Treves, A. (1998). Attractor neural networks storing multiple space representations: A model for hippocampal place fields. Physical Review E, 58(6), 7738–7753.
Ben‐Yishai, R. , Bar‐Or, R. L. , & Sompolinsky, H. (1995). Theory of orientation tuning in visual cortex. Proceedings of the National Academy of Sciences of United States of America, 92(9), 3844–3848. PubMed PMC
Botzung, A. , Denkova, E. , & Manning, L. (2008). Experiencing past and future personal events: Functional neuroimaging evidence on the neural bases of mental time travel. Brain and Cognition, 66, 202–2012. PubMed
Brandon, M. P. , Koenig, J. , Leutgeb, J. K. , & Leutgeb, S. (2014). New and distinct hippocampal place codes are generated in a new environment during septal inactivation. Neuron, 82(4), 789–796. PubMed PMC
Buzsaki, G. (2002). Theta oscillations in the hippocampus. Neuron, 31(3), 325–340. PubMed
Cei, A. , Girardeau, G. , Drieu, C. , Kanbi, K. E. , & Zugaro, M. (2014). Reversed theta sequences of hippocampal cell assemblies during backward travel. Nature Neuroscience, 17(5), 719–724. PubMed
Conklin, J. , & Eliasmith, C. (2005). A controlled attractor network model of path integration in the rat. Journal of Computational Neuroscience, 18:183–203. PubMed
Diba, K. , & Buzsáki, G. (2007). Forward and reverse hippocampal place‐cell sequences during ripples. Nature Neuroscience, 10(10), 1241–1242. PubMed PMC
Dupret, D. , O'neill, J. , & Csicsvari, J. (2013). Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron, 78, 166–180. PubMed PMC
Faisal, A. , Selen, L. P. J. , & Wolpert, D. M. (2008). Noise in the nervous system. Nature Reviews Neuroscience, 9(4), 292–303. PubMed PMC
Fung, C. C. A. , Wong, K. Y. M. , Wang, H. , & Wu, S. (2012). Dynamical synapses enhance neural information processing: Gracefulness, accuracy and mobility. Neural Computation, 24(5), 1147–1185. PubMed
Foster, D. J. , & Wilson, M. A. (2006). Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature, 440(7084), 680–683. PubMed
Foster, D. J. , & Wilson, M. A. (2007). Hippocampal theta sequences. Hippocampus, 17(11), 1093–1099. PubMed
Fyhn, M. , Hafting, T. , Treves, A. , Moser, M. B. , & Moser, E. I. (2007). Hippocampal remapping and grid realignment in entorhinal cortex. Nature, 446(7132), 190–194. PubMed
Gill, P. R. , Mizumori, S. J. Y. , & Smith, D. M. (2011). Hippocampal episode fields develop with learning. Hippocampus, 21(11), 1240–1249. PubMed PMC
Guzman, S. J. , Schlögl, A. , Frotscher, M. , & Jonas, P. (2016). Synaptic mechanisms of pattern completion in the hippocampal CA3 network. Science, 353(6304), 1117–1123. PubMed
Hasselmo, M. E. , Clara, B. , & Bradley, P. W. (2002). A proposed function for hippocampal theta rhythm: Separate phases of encoding and retrieval enhance reversal of prior learning. Neural Computation, 14(4), 793–817. PubMed
Hedrick, K. R. , & Zhang, K. (2016). Megamap: flexible representation of a large space embedded with nonspatial information by a hippocampal attractor network. Journal of neurophysiology, 116(2), 868–891. PubMed PMC
Hopfield, J. J. (2010). Neurodynamics of mental exploration. Proceeding of the National Academy of Science of United States of America, 107(4), 1648–1653. PubMed PMC
Howell, D. (2009). Statistical methods for psychology. (7th edition). Wadsorth, Cengage Learning.
Itskov, V. , Hansel, D. , & Tsodyks, M. (2011). Short‐term facilitation may stabilize parametric working memory trace. Frontiers in Computational Neuroscience, 5, 40. PubMed PMC
Jackson, J. , & Reddish, D. (2007). Network dynamics of hippocampal cell‐assemblies resemble multiple spatial maps within single tasks. Hippocampus, 17, 1209–1229. PubMed
Jezek, K. , Henriksen, E. J. , Treves, A. , Moser, E. I. , & Moser, M. B. (2011). Theta‐paced flickering between place‐cell maps in the hippocampus. Nature, 478(7368), 246–249. PubMed
Kelemen, E. , & Fenton, A. A. (2010). Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biology, 8(6), e1000403. PubMed PMC
Leutgeb, S. , Leutgeb, J. K. , Barnes, C. A. , Moser, E. I. , McNaughton, B. L. , & Moser, M. B. (2005). Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science (New York, N.Y.), 309(5734), 619–623. PubMed
MacDonald, C. J. , Carrow, S. , Place, R. , & Eichenbaum, H. (2013). Distinct hippocampal time cell sequences represent odor memories in immobilized rats. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33(36), 14607–14616. PubMed PMC
MacDonald, C. J. , Lepage, K. Q. , Eden, U. T. , & Eichenbaum, H. (2011). Hippocampal ‘time cells’ bridge the gap in memory for discontiguous events. Neuron, 71(4), 737–749. PubMed PMC
Malvache, A. , Reichinnek, S. , Villette, V. , Haimerl, C. , & Cossart, R. (2016). Awake hippocampal reactivations project onto orthogonal neuronal assemblies. Science, 353(6305), 1280–1283. PubMed
McNaughton, B. L. , Barnes, C. A. , Gerrard, J. L. , Gothard, K. , Jung, M. W. , Knierim, J. J. , … Udrimoti, H. (1996). Deciphering the hippocampal polyglot: the hippocampus as a path integration system. Journal of Experimental Biology, 199(1), 173–185. PubMed
McNaughton, B. L. , & Morris, R. G. M. (1987). Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends in Neurosciences, 10(10), 408–415.
Miles, R. , & Wong, R. K. (1986). Excitatory synaptic interactions between CA3 neurones in the guinea‐pig hippocampus. The Journal of Physiology, 373(1), 397–418. PubMed PMC
Monasson, R. , & Rosay, S. (2015). Transitions between spatial attractors in place‐cell models. Physical Review Letters, 115, 098101. PubMed
Mongillo, G. , Barak, O. , & Tsodyks, M. (2008). Synaptic theory of working memory. Science, 319(5869), 1543–1546. PubMed
Morris, R. G. M. , Garrud, P. , Rawlins, J. N. P. , & O'keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681–683. PubMed
Muller, R. U. , & Kubie, J. L. (1987). The effects of changes in the environment on the spatial firing of hippocampal complex‐spike cells. The Journal of Neuroscience, 7(7), 1951–1968. PubMed PMC
Nakazawa, K. , McHugh, T. J. , Wilson, M. A. , & Tonegawa, S. (2004). NMDA receptors, place cells and hippocampal spatial memory. Nature Reviews Neuroscience, 5(5), 361–372. PubMed
O'Keefe, J. , & Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely‐moving rat. Brain Research, 34(1), 171–175. PubMed
O'Keefe, J. , & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon Press.
Pastalkova, E. , Itskov, V. , Amarasingham, A. , & Buzsaki, G. (2008). Internally generated cell assembly sequences in the rat hippocampus. Science, 321(5894), 1322–1327. PubMed PMC
Pinto, D. , & Ermentrout, G. (2001). Spatially structured activity in synaptically coupled neuronal networks: I. Traveling fronts and pulses. SIAM Journal on Applied Mathematics, 62(1), 206–225.
Pfeiffer, B. E. , & Foster, D. J. (2013). Hippocampal place‐cell sequences depict future paths to remembered goals. Nature, 497(7447), 74–79. PubMed PMC
Redish, A. D. (1999). Beyond the cognitive map: From place cells to episodic memory. MIT Press.
Redish, A. D. , & Touretzky, D. S. (1998). The role of the hippocampus in solving the morris water maze. Neural Computation, 10(1), 73–111. PubMed
Romani, S. , & Tsodyks, M. (2010). Continuous attractors with morphed/correlated maps. Plos Computational Biology, 6(8), e1000869. PubMed PMC
Romani, S. , & Tsodyks, M. (2015). Short‐term plasticity based network model of place cells dynamics. Hippocampus, 25, 94–105. PubMed
Salin, P. A. , Scanziani, M. , Malenka, R. C. , & Nicoll, R. A. (1996). Distinct short‐term plasticity at two excitatory synapses in the hippocampus. Proceedings of the National Academy of Sciences of United States of America, 93(23), 13304–13309. PubMed PMC
Samsonovich, A. , & McNaughton, B. L. (1997). Path integration and cognitive mapping in a continuous attractor neural network model. The Journal of Neuroscience, 17(15), 5900–5920. PubMed PMC
Savin, C. , Dayan, P. , & Lengyel, M. (2014). Optimal recall from bounded metaplastic synapses: Predicting functional adaptations in hippocampal area CA3. PLoS Computational Biology, 10(2), e1003489. PubMed PMC
Scoville, W. B. , & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery & Psychiatry, 20(1), 11–21. PubMed PMC
Selig, D. K. , Nicoll, R. A. , & Malenka, C. (1999). Hippocampal long‐term potentiation preserves the fidelity of postsynaptic responses to presynaptic bursts. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 19(4), 1236–1246. PubMed PMC
Stella, F. , & Treves, A. (2011). Associative memory storage and retrieval: Involvement of theta oscillations in hippocampal information processing. Neural Plasticity, 683961. PubMed PMC
Suddendorf, T. , & Corballis, M. C. (2007). The evolution of foresight: What is mental time travel, and is it unique to humans?. Behavioral and Brain Sciences, 30, 299–351. PubMed
Touretzky, D. S. , & Redish, R. D. (1996). Theory of rodent navigation based on interacting representations of space. Hippocampus, 6(3), 247–270. PubMed
Treves, A. , & Rolls, E. T. (1992). Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus, 2(2), 189–199. PubMed
Tsodyks, M. (1999). Attractor neural network models of spatial maps in hippocampus. Hippocampus, 9(4), 481–489. PubMed
Tsodyks, M. , Pawelzik, K. , & Markram, H. (1998). Neural networks with dynamic synapses. Neural Computation, 10(4), 821–835. PubMed
Tsodyks, M. , & Sejnowski, T. (1995). Associative memory and hippocampal place cells. International Journal of Neural Systems, 6, 81–86.
Tsodyks, M. , Skaggs, W. E. , Sejnowski, T. , & McNaughton, B. L. (1996). Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model. Hippocampus, 6(3), 271–280. PubMed
Vanderwolf, C. H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalography and Clinical Neurophysiology, 26(4), 407–418. PubMed
Wang, Y. , Romani, S. , Lustig, B. , Leonardo, A. , & Pastalkova, E. (2015). Theta sequences are essential for internally generated hippocampal firing fields. Nature Neuroscience, 18(2), 282–288. PubMed
Wikenheiser, A. M. , & Redish, A. D. (2015). Decoding the cognitive map: Ensemble hippocampal sequences and decision making. Current Opinion in Neurobiology, 32, 8–15. PubMed PMC
Wills, T. J. , Lever, C. , Cacucci, F. , Burgess, N. , & O'keefe, J. (2005). Attractor dynamics in the hippocampal representation of the local environment. Science, 308, 873–876. PubMed PMC
Wilson, H. R. , & Cowan, J. D. (1973). A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetik, 13(2), 55–80. PubMed
York, L. C. , & Van Rossum, M. C. W. (2009). Recurrent networks with short term synaptic depression. Journal of Computational Neuroscience, 27(3), 607–620. PubMed
Zhang, K. (1996). Representation of spatial orientation by the intrinsic dynamics of the head‐direction cell ensemble: A theory. Journal of Neuroscience, 16(6), 2112–2126. PubMed PMC