Independent rate and temporal coding in hippocampal pyramidal cells

In the brain, hippocampal pyramidal cells use temporal as well as rate coding to signal spatial aspects of the animal's environment or behaviour. The temporal code takes the form of a phase relationship to the concurrent cycle of the hippocampal electroencephalogram theta rhythm. These two codes could each represent a different variable. However, this requires the rate and phase to vary independently, in contrast to recent suggestions that they are tightly coupled, both reflecting the amplitude of the cell's input. Here we show that the time of firing and firing rate are dissociable, and can represent two independent variables: respectively the animal's location within the place field, and its speed of movement through the field. Independent encoding of location together with actions and stimuli occurring there may help to explain the dual roles of the hippocampus in spatial and episodic memory, or may indicate a more general role of the hippocampus in relational/declarative memory.

[1]  B. McNaughton,et al.  Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model , 1998, Hippocampus.

[2]  N. Schneider,et al.  The Indonesian Throughflow and the Global Climate System , 1998 .

[3]  A. Gordon,et al.  The heat transport of the Indonesian Throughflow and implications for the Indian Ocean heat budget , 2002 .

[4]  Dimitris Menemenlis,et al.  Effects of the Indonesian Throughflow on the Pacific and Indian Oceans , 2002 .

[5]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[6]  A. Gordon,et al.  Pathways of water between the Pacific and Indian oceans in the Indonesian seas , 1996, Nature.

[7]  J. Lisman,et al.  Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. , 2000, Journal of neurophysiology.

[8]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[9]  B. McNaughton,et al.  Experience-dependent, asymmetric expansion of hippocampal place fields. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Arthur J. Mariano,et al.  The Mariano Global Surface Velocity Analysis 1.0. , 1995 .

[11]  ChristodoulouChris,et al.  A spiking neuron model , 2002 .

[12]  Quanan Zheng,et al.  Upwelling along the coasts of Java and Sumatra and its relation to ENSO , 2001 .

[13]  K. Wyrtki Physical oceanography of the Southeast Asian waters , 1961 .

[14]  H. Eichenbaum,et al.  Spatial and behavioral correlates of hippocampal neuronal activity , 1989 .

[15]  F. G. Pike,et al.  Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents , 2000, The Journal of physiology.

[16]  Stephen P. Murray,et al.  Throughflow into the Indian Ocean through the Lombok Strait, January 1985–January 1986 , 1988, Nature.

[17]  F. Syamsudin,et al.  The throughflow within Ombai Strait , 2001 .

[18]  Kevin Vranes,et al.  Temperature variability within Makassar Strait , 2000 .

[19]  B. McNaughton,et al.  Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences , 1996, Hippocampus.

[20]  R. Muller,et al.  A Quarter of a Century of Place Cells , 1996, Neuron.

[21]  C. Wunsch,et al.  Large-Scale Ocean Heat and Freshwater Transports during the World Ocean Circulation Experiment , 2003 .

[22]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[23]  Paul S. Schopf,et al.  Oceanic influences on the seasonal cycle in evaporation over the Indian Ocean , 2001 .

[24]  J. Csicsvari,et al.  Firing rate and theta‐phase coding by hippocampal pyramidal neurons during ‘space clamping’ , 1999, The European journal of neuroscience.

[25]  A. Macdonald,et al.  Property fluxes at 30°S and their implications for the Pacific‐Indian throughflow and the global heat budget , 1993 .

[26]  H. T. Blair,et al.  Hippocampal Place Cells Acquire Location-Specific Responses to the Conditioned Stimulus during Auditory Fear Conditioning , 2003, Neuron.

[27]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[28]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[29]  N. Cohen From Conditioning to Conscious Recollection Memory Systems of the Brain. Oxford Psychology Series, Volume 35. , 2001 .

[30]  Paul E. Robbins,et al.  The dissolved silica budget as a constraint on the meridional overturning circulation of the Indian Ocean , 1997 .

[31]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[32]  Arnold L. Gordon,et al.  Throughflow within Makassar Strait , 1999 .

[33]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

[34]  Carl Wunsch,et al.  Improved estimates of global ocean circulation, heat transport and mixing from hydrographic data , 2000, Nature.

[35]  J. Lisman,et al.  Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. , 1996, Learning & memory.

[36]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 2004, Experimental Brain Research.

[37]  G. Buzsáki,et al.  Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity‐dependent phase‐precession of action potentials , 1998, Hippocampus.

[38]  Arne D. Ekstrom,et al.  NMDA Receptor Antagonism Blocks Experience-Dependent Expansion of Hippocampal “Place Fields” , 2001, Neuron.

[39]  Joseph R. Madsen,et al.  Human theta oscillations exhibit task dependence during virtual maze navigation , 1999, Nature.

[40]  M. Hasselmo,et al.  GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. , 1997, Journal of neurophysiology.

[41]  Michael Recce,et al.  A model of hippocampal function , 1994, Neural Networks.

[42]  B. McNaughton,et al.  Bimodality of theta phase precession in hippocampal place cells in freely running rats. , 2002, Journal of neurophysiology.

[43]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[44]  R. Molcard,et al.  The Indo‐Pacific throughflow in the Timor Passage , 1996 .

[45]  J. Paillard Brain and space , 1991 .

[46]  J. S. Godfrey,et al.  The role of Indonesian throughflow in a global ocean GCM , 1993 .

[47]  G. Buzsáki,et al.  Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells , 2002, Nature.

[48]  B. Goswami,et al.  A dipole mode in the tropical Indian Ocean , 1999, Nature.

[49]  E. Schneider,et al.  The Indonesian Throughflow's Effect on Global Climate Determined from the COLA Coupled Climate System , 2001 .

[50]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[51]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[52]  M. Lengyel,et al.  Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing , 2003, Hippocampus.