Disparate effects of long‐term potentiation on evoked potentials and single CA1 neurons in the hippocampus of anesthetized rats

To examine the effects of long‐term potentiation (LTP) on individual neurons in the intact brain, anesthetized rats were implanted with a recording stereotrode in the right CA1 layer of the hippocampus and a stimulating electrode in the right and left CA3 layers. The evoked and spontaneous firing of single CA1 neurons was characterized before and after LTP of the contralateral (commissural) Schaffer collaterals and again after LTP of the ipsilateral (associational) Schaffer collaterals. Individual CA1 neurons displayed either increases or decreases in evoked and spontaneous firing after LTP. As many as five discriminated cells were recorded simultaneously, and they typically responded discordantly, so that after LTP, firing in some neurons increased while in others it decreased. The response of individual neurons to in vivo LTP may be modulated by heterogeneous synaptic changes on individual and local groups of cells, and by changes in feed‐forward excitation and inhibition provided by local hippocampal circuitry. Hippocampus 10:207–212, 2000 © 2000 Wiley‐Liss, Inc.

[1]  G. Buzsáki.  Long-term potentiation of the commissural path-CA1 pyramidal cell synapse in the hippocampus of the freely moving rat , 1980, Neuroscience Letters.

[2]  J. Sarvey,et al.  Long-term potentiation: studies in the hippocampal slice , 1989, Journal of Neuroscience Methods.

[3]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

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

[5]  H. Eichenbaum,et al.  Cues that hippocampal place cells encode: Dynamic and hierarchical representation of local and distal stimuli , 1997, Hippocampus.

[6]  G. Lynch,et al.  Stable hippocampal long-term potentiation elicited by ‘theta’ pattern stimulation , 1987, Brain Research.

[7]  E. Hargreaves,et al.  An examination of the relations between hippocampal long‐term potentiation, kindling, afterdischarge, and place learning in the water maze , 1993, Hippocampus.

[8]  H. Eichenbaum,et al.  Hippocampus as a memory map: Synaptic plasticity and memory encoding by hippocampal neurons , 1999, Hippocampus.

[9]  David Wood,et al.  Luddites must not block progress in genetics , 1999, Nature.

[10]  Bruce L. McNaughton,et al.  The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records , 1983, Journal of Neuroscience Methods.

[11]  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.

[12]  Sabina Hrabetova,et al.  Long-term potentiation and long-term depression are induced through pharmacologically distinct NMDA receptors 1 Portions of this work were previously published in abstract form [11]. 1 , 1997, Neuroscience Letters.

[13]  G. Buzsáki,et al.  Hippocampal CA1 interneurons: an in vivo intracellular labeling study , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  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.

[15]  J. Eccles,et al.  Hippocampus of the Brain: Recurrent Inhibition in the Hippocampus with Identification of the Inhibitory Cell and its Synapses , 1963, Nature.

[16]  U. Frey,et al.  Synaptic tagging and long-term potentiation , 1997, Nature.

[17]  John O'Keefe,et al.  Place field dynamics and directionality in a spatial memory task , 1998, Brain Research.

[18]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[19]  G. Buzsáki,et al.  Convergence of associational and commissural pathways on CA1 pyramidal cells of the rat hippocampus , 1982, Brain Research.

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

[21]  F. Engert,et al.  Synapse specificity of long-term potentiation breaks down at short distances , 1997, Nature.

[22]  D. Debanne,et al.  Heterogeneity of Synaptic Plasticity at Unitary CA3–CA1 and CA3–CA3 Connections in Rat Hippocampal Slice Cultures , 1999, The Journal of Neuroscience.

[23]  B. Shen,et al.  Long-term potentiation induced by patterned stimulation of the commissural pathway to hippocampal CA1 region in freely moving rats , 1992, Neuroscience.