title: Rapid and continuous modulation of hippocampal network state during exploration of new places.
abstract: Hippocampal information processing is often described as two-state, with a place cell state during movement and a reactivation state during stillness. Relatively little is known about how the network transitions between these different patterns of activity during exploration. Here we show that hippocampal network changes quickly and continuously as animals explore and become familiar with initially novel places. We measured the relationship between moment-by-moment changes in behavior and information flow through hippocampal output area CA1 in rats. We examined local field potential (LFP) patterns, evoked potentials and ensemble spiking and found evidence suggestive of a smooth transition from strong CA3 drive of CA1 activity at low speeds to entorhinal cortical drive of CA1 activity at higher speeds. These changes occurred with changes in behavior on a timescale of less than a second, suggesting a continuous modulation of information processing in the hippocampal circuit as a function of behavioral state.
authors.affiliation: UCSF Center for Integrative Neuroscience and Department of Physiology, University of California San Francisco, San Francisco, California, United States of America ; Department of Electrical and Computer Engineering, Rice University, Houston, Texas, United States of America.
authors.forename: Caleb
authors.initials: C
authors.lastname: Kemere
authors.forename: Margaret F
authors.initials: MF
authors.lastname: Carr
authors.forename: Mattias P
authors.initials: MP
authors.lastname: Karlsson
authors.forename: Loren M
authors.initials: LM
authors.lastname: Frank
mesh_terms: D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D058256:Brain Waves / Q000502:physiology; D056547:CA1 Region, Hippocampal / Q000166:cytology / Q000502:physiology*; D056654:CA3 Region, Hippocampal / Q000166:cytology / Q000502:physiology*; D005071:Evoked Potentials / Q000502:physiology; D005106:Exploratory Behavior / Q000502:physiology*; D007858:Learning / Q000502:physiology; D008297:Male; D009415:Nerve Net / Q000166:cytology / Q000502:physiology*; D009474:Neurons / Q000166:cytology; D051381:Rats; D013997:Time Factors
references.citation: Science. 2006 Aug 25;313(5790):1093-7
references.pmid: 16931756
references.citation: Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14495-500
references.pmid: 17726109
references.citation: J Neurosci. 2010 Sep 1;30(35):11586-604
references.pmid: 20810880
references.citation: Nature. 2003 Jul 31;424(6948):552-6
references.pmid: 12891358
references.citation: Neuron. 1998 Nov;21(5):1123-8
references.pmid: 9856467
references.citation: Nat Neurosci. 2011 Feb;14(2):147-53
references.pmid: 21270783
references.citation: J Neurosci. 2012 May 23;32(21):7373-83
references.pmid: 22623683
references.citation: Neuron. 2000 Jul;27(1):169-78
references.pmid: 10939340
references.citation: J Neurosci. 1996 May 1;16(9):3056-66
references.pmid: 8622135
references.citation: Neuron. 2011 Apr 14;70(1):109-20
references.pmid: 21482360
references.citation: Hippocampus. 2010 Feb;20(2):229-34
references.pmid: 19623610
references.citation: Hippocampus. 2010 Feb;20(2):279-92
references.pmid: 19437417
references.citation: Nat Neurosci. 2009 Jul;12(7):913-8
references.pmid: 19525943
references.citation: Electroencephalogr Clin Neurophysiol. 1978 Sep;45(3):409-11
references.pmid: 79479
references.citation: Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19462-7
references.pmid: 23132944
references.citation: Hippocampus. 2008;18(5):519-29
references.pmid: 18398852
references.citation: J Neurophysiol. 2011 Jun;105(6):2675-86
references.pmid: 21411562
references.citation: J Neurophysiol. 2001 Oct;86(4):2029-40
references.pmid: 11600659
references.citation: Neuroscience. 1994 Oct;62(4):1033-47
references.pmid: 7845584
references.citation: Neuroscience. 2003;116(1):201-11
references.pmid: 12535953
references.citation: J Neurosci. 1999 May 15;19(10):4090-101
references.pmid: 10234037
references.citation: Brain Res. 1986 Nov 29;398(2):242-52
references.pmid: 3026567
references.citation: Neuron. 2002 Jan 31;33(3):325-40
references.pmid: 11832222
references.citation: Electroencephalogr Clin Neurophysiol. 1969 Apr;26(4):407-18
references.pmid: 4183562
references.citation: Neuroscience. 2001;106(1):43-53
references.pmid: 11564415
references.citation: Nature. 2006 Mar 30;440(7084):680-3
references.pmid: 16474382
references.citation: Neuron. 2008 Jan 24;57(2):290-302
references.pmid: 18215625
references.citation: Nature. 2012 Nov 22;491(7425):547-53
references.pmid: 23172213
references.citation: J Comp Physiol Psychol. 1975 Jan;88(1):300-23
references.pmid: 235571
references.citation: Brain Res. 1983 Oct;287(2):139-71
references.pmid: 6357356
references.citation: J Neurosci. 2008 Dec 24;28(52):14271-81
references.pmid: 19109508
references.citation: J Neurosci Methods. 2004 Feb 15;133(1-2):161-72
references.pmid: 14757357
references.citation: PLoS One. 2011;6(6):e21408
references.pmid: 21731735
references.citation: Neuron. 2000 Nov;28(2):585-94
references.pmid: 11144366
references.citation: J Neurosci. 1995 Jan;15(1 Pt 1):47-60
references.pmid: 7823151
references.citation: J Neurosci. 2004 Sep 1;24(35):7681-9
references.pmid: 15342735
references.citation: Eur J Neurosci. 1998 Feb;10(2):464-77
references.pmid: 9749709
references.citation: Neuron. 2008 Jan 24;57(2):303-13
references.pmid: 18215626
references.citation: Cereb Cortex. 2012 Oct;22(10):2404-14
references.pmid: 22079925
references.citation: Behav Biol. 1973 Apr;8(4):461-84
references.pmid: 4350255
references.citation: Neuron. 2009 Jun 25;62(6):781-7
references.pmid: 19555647
references.citation: Nat Neurosci. 2013 Mar;16(3):264-6
references.pmid: 23396101
references.citation: Science. 2008 Feb 29;319(5867):1260-4
references.pmid: 18218862
references.citation: Neuron. 2004 Jun 10;42(5):803-15
references.pmid: 15182719
references.citation: Hippocampus. 2012 May;22(5):1164-75
references.pmid: 21748821
references.citation: Neuroscience. 1989;31(3):551-70
references.pmid: 2687720
references.citation: Hippocampus. 2008;18(4):340-8
references.pmid: 18081172
references.citation: Science. 1994 Jul 29;265(5172):676-9
references.pmid: 8036517
references.citation: Neuron. 2012 Aug 23;75(4):700-13
references.pmid: 22920260
references.citation: Science. 1993 Feb 26;259(5099):1324-6
references.pmid: 8446900
references.citation: Nat Neurosci. 2008 Feb;11(2):209-15
references.pmid: 18193040
references.citation: Exp Brain Res. 1983;52(1):41-9
references.pmid: 6628596
references.citation: J Physiol. 1973 Jul;232(2):331-56
references.pmid: 4727084
references.citation: Exp Brain Res. 1981;41(3-4):399-410
references.pmid: 7215500
references.citation: Science. 1993 Aug 20;261(5124):1055-8
references.pmid: 8351520
references.citation: J Neurophysiol. 1978 May;41(3):716-32
references.pmid: 207830
references.citation: Neuron. 2011 Jul 14;71(1):155-65
references.pmid: 21745645
references.citation: Nat Neurosci. 2007 Oct;10(10):1241-2
references.pmid: 17828259
references.citation: Nature. 2009 Nov 19;462(7271):353-7
references.pmid: 19924214
references.citation: Hippocampus. 1996;6(4):347-470
references.pmid: 8915675
references.citation: J Neurosci. 2007 Nov 7;27(45):12176-89
references.pmid: 17989284
references.citation: Neuron. 2009 Oct 29;64(2):267-80
references.pmid: 19874793
references.citation: J Neurosci. 1994 Jun;14(6):3898-914
references.pmid: 8207494
references.citation: PLoS One. 2009;4(5):e5494
references.pmid: 19424438