Experience-Dependent Changes in Extracellular Spike Amplitude May Reflect Regulation of Dendritic Action Potential Back-Propagation in Rat Hippocampal Pyramidal Cells

Activity-dependent attenuations in extracellular spike amplitude have been shown to correlate with a decrease in the effectiveness with which somatic action potentials back-propagate into the dendritic arbor of hippocampal pyramidal cells. In this paper we demonstrate that activity-dependent attenuations in amplitude occur during behavior and that the amount of attenuation is reduced with an animal's experience in an environment. The observed reductions are caused by an animal's experience within a specific environmental context, are dependent on functional NMDA receptors, and are accompanied by an increase in the effective coupling of pyramidal cells and interneurons. These results provide an important step in linking together in vivostudies with in vitro data and suggest that mechanisms of plasticity engaged during behavior may be sufficient to alter the biophysical and integrative properties of hippocampal pyramidal cells.

[1]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[2]  W. Chambers,et al.  Reflexes involving triceps surae from the ankle joint of the cat. , 1973, Experimental neurology.

[3]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

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

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

[6]  G. Lynch,et al.  Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5 , 1986, Nature.

[7]  W. N. Ross,et al.  The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons , 1992, Nature.

[8]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[9]  M. Bear,et al.  Synaptic plasticity: LTP and LTD , 1994, Current Opinion in Neurobiology.

[10]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

[11]  N. Spruston,et al.  Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. , 1995, Science.

[12]  D. Johnston,et al.  Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. , 1995, Science.

[13]  P Andersen,et al.  Brain temperature and hippocampal function , 1995, Hippocampus.

[14]  G. Buzsáki,et al.  Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  W. N. Ross,et al.  IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons. , 1996, Journal of neurophysiology.

[16]  D. Johnston,et al.  Active properties of neuronal dendrites. , 1996, Annual review of neuroscience.

[17]  L. F. Abbott,et al.  A Model of Spatial Map Formation in the Hippocampus of the Rat , 1999, Neural Computation.

[18]  J. Sweatt,et al.  A biochemist's view of long-term potentiation. , 1996, Learning & memory.

[19]  M. Hasselmo,et al.  NMDA-dependent modulation of CA1 local circuit inhibition , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  K. I. Blum,et al.  Impaired Hippocampal Representation of Space in CA1-Specific NMDAR1 Knockout Mice , 1996, Cell.

[21]  M. Sarter,et al.  Cognitive functions of cortical acetylcholine: toward a unifying hypothesis , 1997, Brain Research Reviews.

[22]  L. Bianchi,et al.  Glutamatergic Modulation of Cortical Acetylcholine Release in the Rat: A Combined In Vivo Microdialysis, Retrograde Tracing and lmmunohistochemical Study , 1997, The European journal of neuroscience.

[23]  D. Johnston,et al.  K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons , 1997, Nature.

[24]  N. Spruston,et al.  Prolonged Sodium Channel Inactivation Contributes to Dendritic Action Potential Attenuation in Hippocampal Pyramidal Neurons , 1997, The Journal of Neuroscience.

[25]  D. Johnston,et al.  Slow Recovery from Inactivation of Na+ Channels Underlies the Activity-Dependent Attenuation of Dendritic Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1997, The Journal of Neuroscience.

[26]  W. N. Ross,et al.  Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. , 1997, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[28]  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.

[29]  D. Johnston,et al.  Downregulation of Transient K+ Channels in Dendrites of Hippocampal CA1 Pyramidal Neurons by Activation of PKA and PKC , 1998, The Journal of Neuroscience.

[30]  J. Csicsvari,et al.  Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus an Ensemble Approach in the Behaving Rat , 1998, Neuron.

[31]  C Kentros,et al.  Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. , 1998, Science.

[32]  R. Zucker,et al.  Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. , 1999, Journal of neurophysiology.

[33]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[34]  D. Johnston,et al.  Neuromodulation of dendritic action potentials. , 1999, Journal of neurophysiology.

[35]  D. Tank,et al.  In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons , 1999, Nature Neuroscience.

[36]  D. Debanne,et al.  The role of dendritic filtering in associative long-term synaptic plasticity. , 1999, Learning & memory.

[37]  M. Quirk,et al.  Interaction between spike waveform classification and temporal sequence detection , 1999, Journal of Neuroscience Methods.

[38]  M. Quirk,et al.  Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields , 2000, Neuron.

[39]  M. Wilson,et al.  Trajectory Encoding in the Hippocampus and Entorhinal Cortex , 2000, Neuron.

[40]  Stefan Offermanns,et al.  Calcium-Dependent Persistent Facilitation of Spike Backpropagation in the CA1 Pyramidal Neurons , 2000, The Journal of Neuroscience.

[41]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.