Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats

SummaryRecordings were taken from single neurons in the hippocampus and dentate gyrus of rats during walking and urethane anesthesia. Firing histograms for these cells were constructed as a function of the phase of the concurrent extracellularly recorded hippocampal slow wave theta rhythm. Care was taken to be sure of the site of recording of the theta rhythm and its phase with respect to a reliable reference, so that comparisons of the phases of firing could be made across animals. The firing of most of these neurons is deeply modulated as a function of the phase of the theta rhythm. This is true whether the theta rhythm occurs during walking or during urethane anesthesia, but for some types of cells the mean phases of firing are different in the two types of theta rhythm. During walking, pyramidal cells and interneurons in all hippocampal subregions and dentate granule cells have a maximum probability of firing near the positive peak of the theta rhythm recorded in the outer molecular layer of the dentate (dentate theta). During urethane anesthesia, the maximum firing probability for interneurons in CA1 and for dentate granule cells occurs near the negative peak of the dentate theta, while the phases of maximum firing for pyramidal cells and interneurons in CA3 and CA4 become widely distributed. The phases of maximum firing of pyramidal cells in CA1 are, if anything, more narrowly distributed around the positive peak of the dentate theta during urethane anesthesia than during walking. These differences in the firing of hippocampal cells during walking and urethane anesthesia represent some of the differences in cellular mechanisms distinguishing two kinds of hippocampal theta rhythm.

[1]  Bernice W. Polemis.  Nonparametric Statistics for the Behavioral Sciences , 1959 .

[2]  P. Andersen,et al.  Excitatory synapses on hippocampal apical dendrites activated by entorhinal stimulation. , 1966, Acta physiologica Scandinavica.

[3]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[4]  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.

[5]  J. Winson,et al.  Patterns of hippocampal theta rhythm in the freely moving rat. , 1974, Electroencephalography and clinical neurophysiology.

[6]  C. H. Vanderwolf,et al.  Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: Relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital , 1975, Experimental Neurology.

[7]  Jonathan Winson,et al.  Hippocampal theta rhythm. I. Depth profiles in the curarized rat , 1976, Brain Research.

[8]  P. Coyle.  Hippocampal spike-slow wave phase relations after midbrain transection in rabbits , 1976, Experimental Neurology.

[9]  S. Fox,et al.  Hippocampal field potentials evoked by stimulation of multiple limbic structures in freely moving rats , 1979, Neuroscience.

[10]  R. Chronister,et al.  Organization of projection neurons of the hippocampus , 1979, Experimental Neurology.

[11]  G. Lynch,et al.  A microdrive for use with glass or metal microelectrodes in recording from freely-moving rats. , 1979, Electroencephalography and clinical neurophysiology.

[12]  J. B. Ranck,et al.  Generation of theta rhythm in medial entorhinal cortex of freely moving rats , 1980, Brain Research.

[13]  J. B. Ranck,et al.  Hippocampal excitability phase-locked to the theta rhythm in walking rats , 1980, Experimental Neurology.

[14]  N. Brecha,et al.  Localization of enkephalin‐like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus , 1981, The Journal of comparative neurology.

[15]  H. Eichenbaum,et al.  Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  B. H. Bland,et al.  theta-Cells in CA1 and dentate layers of hippocampal formation: relations to slow-wave activity and motor behavior in the freely moving rabbit. , 1982, Journal of neurophysiology.

[17]  G. Buzsáki,et al.  Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat , 1983, Brain Research.

[18]  R. F. Thompson,et al.  Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. , 1983, Journal of neurophysiology.

[19]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[20]  G. Lynch,et al.  Dentate granule cells in the rat hippocampal formation have the behavioral characteristics of theta neurons , 1983, Brain Research.

[21]  Theta rhythm related hippocampal cell discharges in the urethane anaesthetized rat: evidence for a predominant entorhinal input. , 1983, Electroencephalography and clinical neurophysiology.

[22]  B. H. Bland,et al.  The pharmacology of hippocampal theta cells: Evidence that the sensory processing correlate is cholinergic , 1984, Brain Research.

[23]  S. Fox,et al.  Hippocampal excitability related to the phase of the theta rhythm in urethanized rats , 1984, Brain Research.

[24]  P. Andersen,et al.  Automated analysis of rhythmicity of physiologically identified hippocampal formation neurons , 2004, Experimental Brain Research.

[25]  J. B. Ranck,et al.  Electrophysiological characteristics of hippocampal complex-spike cells and theta cells , 2004, Experimental Brain Research.

[26]  J. Holsheimer.  Generation of theta activity (RSA) in the cingulate cortex of the rat , 2004, Experimental Brain Research.

[27]  P. Andersen,et al.  Mode of activation of hippocampal pyramidal cells by excitatory synapses on dendrites , 2004, Experimental Brain Research.