Abstract
Based on our previously published study, in this chapter, we discuss the interaction between the hippocampus (CA1) and primary visual cortex (V1) in the acquisition and consolidation of memories with an emphasis upon how this study supports, and expands upon, contemporary memory theories. Both CA1 and V1 neurons were shown to contribute to the acquisition of hippocampal-dependent episodic memory and to the memory consolidation process during slow-wave sleep. V1 neurons also participate in hippocampal-independent remote memory function following consolidation. Thus, V1 neurons appear to be tuned to both external stimuli and internal memories. These data not only support key elements of contemporary memory theories but also provide fresh, new insights into the consolidation process. Our findings also raise important questions with regard to the distinctions between sensory and memory circuits.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992;99:195–231.
Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry. 1957;20:11–21.
Corkin S. What’s new with the amnesic patient H.M.? Nat Rev Neurosci. 2002;3:153–60.
Marr D. A theory for cerebral neocortex. Proc R Soc Lond B Biol Sci. 1970;176(43):161–234.
Marr D. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci. 1971;262(841):23–81.
McClelland JL, McNaughton BL, O’Reilly RC. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev. 1995;102:419–57.
Teyler TJ, Rudy JW. The hippocampal indexing theory and episodic memory: updating the index. Hippocampus. 2007;17:1158–69.
Buzsaki G. Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience. 1989;31:551–70.
Buzsaki G. The hippocampo-neocortical dialogue. Cereb Cortex. 1996;6:81–92.
Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, et al. Schemas and memory consolidation. Science. 2007;316(5821):76–82.
Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C, et al. Schema-dependent gene activation and memory encoding in neocortex. Science. 2011;333(6044):891–5.
Teyler TJ, DiScenna P. The role of hippocampus in memory: a hypothesis. Neurosci Biobehav Rev. 1985;9(3):377–89.
Teyler TJ, DiScenna P. The hippocampal memory indexing theory. Behav Neurosci. 1986;100(2):147–54.
O’Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34:171–5.
O’Keefe J. Place units in the hippocampus of the freely moving rat. Exp Neurol. 1976;51(1):78–109.
Itskov V, Curto C, Pastalkova E, Buzsáki G. Cell assembly sequences arising from spike threshold adaptation keep track of time in the hippocampus. J Neurosci. 2011;31(8):2828–34.
MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron. 2011;71(4):737–49.
Buzsáki G. Theta oscillations in the hippocampus. Neuron. 2002;33(3):325–40.
Wiltgen BJ, Brown RAM, Talton LE, Silva AJ. New circuits for old memories: the role of the neocortex in consolidation. Neuron. 2004;44(1):101–8.
Frankland PW, Bontempi B. The organization of recent and remote memories. Nat Rev Neurosci. 2005;6:119–30.
Maviel T, Durkin TP, Menzaghi F, Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science. 2004;305(5680):96–9.
Takehara K, Kawahara S, Kirino Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci. 2003;23(30):9897–905.
Lopez-Aranda MF, Lopez-Tellez JF, Navarro-Lobato I, Masmudi-Martin M, Gutierrez A, Khan ZU. Role of layer 6 of V2 visual cortex in object-recognition memory. Science. 2009;325:87–9.
Yao H, Shi L, Han F, Gao H, Dan Y. Rapid learning in cortical coding of visual scenes. Nat Neurosci. 2007;10:772–8.
Xu S, Jiang W, Poo MM, Dan Y. Activity recall in a visual cortical ensemble. Nat Neurosci. 2012;15:449–55, S1–2.
Wheeler ME, Petersen SE, Buckner RL. Memory’s echo: vivid remembering reactivates sensory-specific cortex. Proc Natl Acad Sci U S A. 2000;97:11125–9.
Kosslyn SM, Pascual-Leone A, Felician O, Camposano S, Keenan JP, Thompson WL, et al. The role of area 17 in visual imagery: convergent evidence from PET and rTMS. Science. 1999;284:167–70.
Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2007;10:100–7.
Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H. The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron. 1999;23:209–26.
Ferbinteanu J, Kennedy PJ, Shapiro ML. Episodic memory–from brain to mind. Hippocampus. 2006;16:691–703.
Knierim JJ, Lee I, Hargreaves EL. Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus. 2006;16:755–64.
McNaughton BL, Barnes CA, O’Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res. 1983;52:41–9.
Wilson MA, McNaughton BL. Dynamics of the hippocampal ensemble code for space. Science. 1993;261:1055–8.
Muller R. A quarter of a century of place cells. Neuron. 1996;17:813–22.
Muller RU, Kubie JL. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci. 1987;7:1951–68.
Knierim JJ. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci. 2002;22:6254–64.
Lee I, Yoganarasimha D, Rao G, Knierim JJ. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature. 2004;430:456–9.
Miller MW, Vogt BA. Direct connections of rat visual cortex with sensory, motor, and association cortices. J Comp Neurol. 1984;226:184–202.
Lavenex P, Amaral DG. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus. 2000;10:420–30.
Alvarez P, Squire LR. Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci U S A. 1994;91:7041–5.
Kali S, Dayan P. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat Neurosci. 2004;7:286–94.
Skaggs WE, McNaughton BL, Gothard KM, Markus EJ. An information-theoretic approach to deciphering the hippocampal code, Advances in neural processing systems. San Mateo: Morgan Kaufmann; 1993. p. 1030–7.
Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265:676–9.
Lee AK, Wilson MA. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron. 2002;36:1183–94.
Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271:1870–3.
Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 1999;19:9497–507.
Cossart R, Aronov D, Yuste R. Attractor dynamics of network UP states in the neocortex. Nature. 2003;423:283–8.
Shu Y, Hasenstaub A, McCormick DA. Turning on and off recurrent balanced cortical activity. Nature. 2003;423:288–93.
Sanchez-Vives MV, McCormick DA. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 2000;3:1027–34.
Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A. 2003;100:13638–43.
Volgushev M, Chauvette S, Mukovski M, Timofeev I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations [corrected]. J Neurosci. 2006;26:5665–72.
Amzica F, Steriade M. Cellular substrates and laminar profile of sleep K-complex. Neuroscience. 1998;82:671–86.
Steriade M, Timofeev I, Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol. 2001;85:1969–85.
Hahn TT, Sakmann B, Mehta MR. Phase-locking of hippocampal interneurons’ membrane potential to neocortical up-down states. Nat Neurosci. 2006;9:1359–61.
Hahn TT, Sakmann B, Mehta MR. Differential responses of hippocampal subfields to cortical up-down states. Proc Natl Acad Sci U S A. 2007;104:5169–74.
Isomura Y, Sirota A, Ozen S, Montgomery S, Mizuseki K, Henze DA, et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron. 2006;52:871–82.
Amzica F, Steriade M. Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation. J Neurosci. 1995;15(6):4658–77.
Amzica F, Steriade M. Short- and long-range neuronal synchronization of the slow (<1 Hz) cortical oscillation. J Neurophysiol. 1995;73(1):20–38.
Steriade M, Amzica F. Slow sleep oscillation, rhythmic K-complexes, and their paroxysmal developments. J Sleep Res. 1998;7 Suppl 1:30–5.
Harris JA, Petersen RS, Diamond ME. The cortical distribution of sensory memories. Neuron. 2001;30:315–8.
MacLean JN, Watson BO, Aaron GB, Yuste R. Internal dynamics determine the cortical response to thalamic stimulation. Neuron. 2005;48:811–23.
Luczak A, Barthó P, Marguet SL, Buzsáki G, Harris KD. Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A. 2007;104(1):347–52.
Luczak A, Bartho P, Harris KD. Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron. 2009;62:413–25.
Girman SV, Sauve Y, Lund RD. Receptive field properties of single neurons in rat primary visual cortex. J Neurophysiol. 1999;82:301–11.
Niell CM, Stryker MP. Highly selective receptive fields in mouse visual cortex. J Neurosci. 2008;28:7520–36.
Niell CM, Stryker MP. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron. 2010;65:472–9.
Olshausen BA, Field DJ. What is the other 85% of V1 doing? In: Sejnowski TJ, van Hemmen L, editors. Problems in systems neuroscience. Oxford: Oxford University Press; 2004.
Lee TS, Yang CF, Romero RD, Mumford D. Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency. Nat Neurosci. 2002;5:589–97.
Gilbert CD, Sigman M. Brain states: top-down influences in sensory processing. Neuron. 2007;54:677–96.
Gregoriou GG, Gotts SJ, Zhou H, Desimone R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science. 2009;324:1207–10.
Shuler MG, Bear MF. Reward timing in the primary visual cortex. Science. 2006;311:1606–9.
Vaudano E, Legg CR, Glickstein M. Afferent and efferent connections of temporal association cortex in the rat: a horseradish peroxidase study. Eur J Neurosci. 1991;3:317–30.
Furtak SC, Wei SM, Agster KL, Burwell RD. Functional neuroanatomy of the parahippocampal region in the rat: the perirhinal and postrhinal cortices. Hippocampus. 2007;17:709–22.
Rolls ET. Hippocampo-cortical and cortico-cortical backprojections. Hippocampus. 2000;10:380–8.
Insausti R, Herrero MT, Witter MP. Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus. 1997;7:146–83.
Burwell RD, Amaral DG. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol. 1998;398:179–205.
Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Amsterdam: Elsevier; 2007.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer Science+Business Media New York
About this chapter
Cite this chapter
Haggerty, D.C., Ji, D. (2015). Coordinated Sequence Replays Between the Visual Cortex and Hippocampus. In: Tatsuno, M. (eds) Analysis and Modeling of Coordinated Multi-neuronal Activity. Springer Series in Computational Neuroscience, vol 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1969-7_9
Download citation
DOI: https://doi.org/10.1007/978-1-4939-1969-7_9
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4939-1968-0
Online ISBN: 978-1-4939-1969-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)