Spatial organization of physiological activity in the hippocampal region: relevance to memory formation.

Based on a review of anatomical and physiological findings, we suggest that the hippocampus may be viewed as a positive feedback device (autoassociator), which is capable of modifying the activity of the neocortical neurons. We examine the three-dimensional organization of evoked and spontaneous physiological patterns of the hippocampus and suggest rules how these patterns emerge during different behaviors from a hard-wired structural network. The high spatial coherence of theta activity is due to an external pacemaker, while the high synchrony of population bursts underlying hippocampal sharp waves is explained by the similar probability of recruitment of neurons by the burst-initiator cells along the whole extent of the hippocampus. We suggest that the burst-initiator cells are a group of CA3 neurons whose excitability is increased by a transient potentiation action of the neocortical activity during theta-concurrent exploratory behaviors. We hypothesize that sharp wave-concurrent population bursts result in a highly synchronous hippocampal output, converging preferentially on those entorhinal neurons which were instrumental in the creation of the burst-initiator neurons. The feedback action of population activity thus provides a selective mechanism for potentiation of connections between information-carrying neurons in the hippocampus and entorhinal cortex. The state-dependent operations of the anatomical hardware also point to the importance and advantage of studying the physiological activity of the intact brain.

[1]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

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

[3]  T. Teyler,et al.  The hippocampal memory indexing theory. , 1986, Behavioral neuroscience.

[4]  L. Squire Mechanisms of memory. , 1986, Lancet.

[5]  C. H. Vanderwolf Cerebral activity and behavior: control by central cholinergic and serotonergic systems. , 1988, International review of neurobiology.

[6]  G. Buzsáki,et al.  Neuronal activity in the subcortically denervated hippocampus: A chronic model for epilepsy , 1989, Neuroscience.

[7]  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.

[8]  T. Sejnowski,et al.  Commissural synapses, but not mossy fiber synapses, in hippocampal field CA3 exhibit associative long-term potentiation and depression , 1989, Brain Research.

[9]  D. Amaral,et al.  Memory and the Hippocampus , 1989 .

[10]  G. Buzsáki Feed-forward inhibition in the hippocampal formation , 1984, Progress in Neurobiology.

[11]  G. Buzsáki,et al.  Behavioral dependence of the electrical activity of intracerebrally transplanted fetal hippocampus , 1987, Brain Research.

[12]  J. Winson,et al.  Neuronal transmission through hippocampal pathways dependent on behavior. , 1978, Journal of neurophysiology.

[13]  G. Buzsáki What does the “LTP Model of Memory” Model? , 1985 .

[14]  G. K. Smith,et al.  Spontaneous EEG spikes in the normal hippocampus. II. Relations to synchronous burst discharges. , 1988, Electroencephalography and clinical neurophysiology.

[15]  R. Traub,et al.  Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. , 1988, Journal of neurophysiology.

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

[17]  W. R. Adey,et al.  Sleep of unrestrained chimpanzee: cortical and subcortical recordings. , 1969, Experimental neurology.

[18]  G. K. Smith,et al.  Spontaneous EEG spikes in the normal hippocampus. V. Effects of ether, urethane, pentobarbital, atropine, diazepam and bicuculline. , 1988, Electroencephalography and clinical neurophysiology.

[19]  Brian H. Bland,et al.  Intracellular records of carbachol-induced theta rhythm in hippocampal slices , 1988, Brain Research.

[20]  B. McNaughton,et al.  Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents , 1978, Brain Research.

[21]  O. Prohaska,et al.  Multisite recording of brain field potentials and unit activity in freely moving rats , 1989, Journal of Neuroscience Methods.

[22]  D. Amaral,et al.  Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat , 1990, The Journal of comparative neurology.

[23]  F. Freemon,et al.  Electrical activity of human limbic system during sleep. , 1970, Comprehensive psychiatry.

[24]  B. H. Bland The physiology and pharmacology of hippocampal formation theta rhythms , 1986, Progress in Neurobiology.

[25]  G. K. Smith,et al.  Spontaneous EEG spikes in the normal hippocampus. I. Behavioral correlates, laminar profiles and bilateral synchrony. , 1987, Electroencephalography and clinical neurophysiology.

[26]  L. Kellényi,et al.  Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: Current-source density analysis, effects of urethane and atropine , 1986, Brain Research.

[27]  N. Tamamaki,et al.  Three-dimensional analysis of the whole axonal arbors originating from single CA2 pyramidal neurons in the rat hippocampus with the aid of a computer graphic technique , 1988, Brain Research.

[28]  R. Douglas,et al.  Long lasting synaptic potentiation in the rat dentate gyrus following brief high frequency stimulation , 1977, Brain Research.

[29]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[30]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[31]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

[32]  R. Nicoll The septo-hippocampal projection: a model cholinergic pathway , 1985, Trends in Neurosciences.

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

[34]  G. Buzsáki Hippocampal sharp waves: Their origin and significance , 1986, Brain Research.

[35]  F. H. Lopes da Silva,et al.  Spectral characteristics of the hippocampal EEG in the freely moving rat. , 1982, Electroencephalography and clinical neurophysiology.

[36]  J. Morley,et al.  Flavour modulates the antidipsogenic effect of substance P , 1981, Brain Research.

[37]  R. Traub,et al.  Model of the origin of rhythmic population oscillations in the hippocampal slice. , 1989, Science.

[38]  E. Grastyán,et al.  Hippocampal electrical activity during the development of conditioned reflexes. , 1959, Electroencephalography and clinical neurophysiology.

[39]  Lorand Kellenyi,et al.  Changes in neuronal transmission in the rat hippocampus during behavior , 1981, Brain Research.

[40]  H. Petsche,et al.  [The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells]. , 1962, Electroencephalography and clinical neurophysiology.