Physiology of the hippocampus and related structures.

Despite the large number of studies on all aspects of the hippocampus, the function of this structure is still an enigma. In our view multidisciplinary studies of input-output relations integrated with behavioral analytical inves­ tigations hold the greatest promise for a solution to this problem. Therefore, this review is dedicated to the basic physiology of the hippocampus seen as a group of input-output subsystems. The first several sections deal with the functional anatomy and electro­ physiology. This subject receives more intensive treatment in those sections where recent anatomical data obtained with tracer techniques have pro­ vided significant advances. In the second half of the review, hippocampal­ behavior correlates are dealt with. The insight of the authors into these aspects is here given precedence over a detailed review of the extensive literature. The treatment of transmitters and pharmacological aspects is omitted here in view of the recent comprehensive review of Storm-Mathisen ( 194). Several reviews of the physiology of the hippocampus have been published. A classic is that of Brodal (39). The last physiological review is that of Green (86). Since then there have appeared reviews on the phar­ macology of the electrical activity of the hippocampus ( 196); on the physi­ ology of cellular processes (189); and on behavioral correlates of hippocam­ pal function (4, 63, 1l3, 141). The comprehensive book of Isaacson ( 103) gives a survey of the limbic system. A collection of papers on several aspects of hippocampal structure and physiology, its relation to behavior, its devel­ opment and neuroendocrinology has been edited recently by Isaacson & Pribram ( 104). A book covering the Russian literature on the hippocampus has also appeared (76).

[1]  H. Teitelbaum,et al.  Relationship between hippocampal theta activity and running speed in the rat. , 1975, Journal of comparative and physiological psychology.

[2]  C. H. Vanderwolf,et al.  Chapter 8 – Diencephalic, Hippocampal, and Neocortical Mechanisms in Voluntary Movement1 , 1973 .

[3]  P. Maclean,et al.  Photically sustained on-responses of units in posterior hippocampal gyrus of awake monkey. , 1968, Journal of neurophysiology.

[4]  F. Reinoso-suárez,et al.  Differential efferent connections of the brain stem to the hippocampus in the cat , 1977, Brain Research.

[5]  P. Andersen,et al.  Activation of the field CA-1 of the hippocampus by septal stimulation. , 1961, Acta physiologica Scandinavica.

[6]  Jonathan Winson,et al.  Hippocampal theta rhythm. II. Depth profiles in the freely moving rabbit , 1976, Brain Research.

[7]  S. Landis,et al.  Afferents to the hippocampus of the rat studied with the method of retrograde transport of horseradish peroxidase. , 1974, Brain research.

[8]  E. K. Michal Effects of limbic lesions on behavior sequences and courtship behavior of male rats (Rattus norvegicus). , 1973, Behaviour.

[9]  Judith A. F. Cruce,et al.  An autoradiographic study of the projections of the mammillothalamic tract in the rat , 1975, Brain Research.

[10]  J. B. Angevine Development of the Hippocampal Region , 1975 .

[11]  V. B. Domesick Projections from the cingulate cortex in the rat. , 1969, Brain research.

[12]  T. Blackstad Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination , 1956, The Journal of comparative neurology.

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

[14]  J J Miller,et al.  The hippocampal control of neuronal discharges in the septum of the rat , 1974, The Journal of physiology.

[15]  W. Kilmer,et al.  A model of hippocampal CA3 circuitry. , 1970, The International journal of neuroscience.

[16]  J. D. Green,et al.  Hippocampal electrical activity in arousal. , 1954, Journal of neurophysiology.

[17]  L. E. White,et al.  The midline septum telencephali: A raphe , 1976, Experimental Neurology.

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

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

[20]  Donald O. Walter,et al.  Mass action in the nervous system , 1975 .

[21]  J. Defrance,et al.  Fimbria input to the nucleus accumbens septi , 1975, Brain Research.

[22]  Avarez-Leefmans Fj,et al.  Proceedings: Influences of the septum on the hippocampal dentate area which are unaccompanied by field potentials. , 1975 .

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

[24]  A. R. Gardner-Medwin,et al.  The effect of synaptic activation on the extracellular potassium concentration in the hippocampal dentate area, in vitro , 1976, Brain Research.

[25]  F. Bloom,et al.  Discharge patterns of cat raphe neurons during sleep and waking. , 1974, Brain research.

[26]  B B Brown,et al.  Frequency and phase of hippocampal theta activity in the spontaneously behaving cat. , 1968, Electroencephalography and clinical neurophysiology.

[27]  C. Leonard,et al.  Connections of the median and dorsal raphe nuclei in the rat: An autoradiographic and degeneration study , 1974, The Journal of comparative neurology.

[28]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. II. Hippocampal slow waves and theta cell firing during bar pressing and other behaviors. , 1973, Experimental neurology.

[29]  J. Defrance,et al.  Electrophysiological analysis of the hippocampal-septal projections: II. Functional characteristics , 1973, Experimental Brain Research.

[30]  C. H. Vanderwolf,et al.  Hippocampal EEG and behavior: changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. , 1973, Behavioral biology.

[31]  D. Olton,et al.  Animal Behavior Processes , 2022 .

[32]  G. Danscher,et al.  Distribution of heavy metals in the hippocampal region of the guinea pig , 1974, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

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

[34]  A. Sano,et al.  Eye movements and hippocampal theta activity in rats. , 1973, Electroencephalography and clinical neurophysiology.

[35]  A. Brodal The hippocampus and the sense of smell; a review. , 1947, Brain : a journal of neurology.

[36]  L. Nadel,et al.  Fornix lesions selectively abolish place learning in the rat , 1975, Experimental Neurology.

[37]  Y Fujita,et al.  INTRACELLULAR RECORDS FROM HIPPOCAMPAL PYRAMIDAL CELLS IN RABBIT DURING THETA RHYTHM ACTIVITY. , 1964, Journal of neurophysiology.

[38]  Kandel Er,et al.  Cellular and integrative properties of the hippocampal pyramidal cell and the comparative electrophysiology of cortical neurons. , 1968 .

[39]  E. Fifková,et al.  Two types of terminal degeneration in the molecular layer of the dentate fascia following lesions of the entorhinal cortex. , 1975, Brain research.

[40]  W. Nauta,et al.  A Comparison of the Distribution of the fornix system in the rat, guinea pig, cat, and monkey , 1959, The Journal of comparative neurology.

[41]  P. J. Stoll,et al.  A neural network with a background level of excitation in the cat hippocampus. , 1973, The International journal of neuroscience.

[42]  J. Storm-Mathisen Localization of transmitter candidates in the brain: the hippocampal formation as a model , 1977, Progress in Neurobiology.

[43]  W. Nauta An experimental study of the fornix system in the rat , 1956, The Journal of comparative neurology.

[44]  B. Cragg,et al.  Responses of the hippocampus to stimulation of the olfactory bulb and of various afferent nerves in five mammals. , 1960, Experimental Neurology.

[45]  A. Siegel,et al.  Efferent connections of the hippocampal formation in the rat , 1977, Brain Research.

[46]  Black Ah,et al.  Electrical activity of the hippocampus and cortex in dogs operantly trained to move and to hold still. , 1972 .

[47]  L. Jarrard,et al.  Open-field behavior of hippocampal-lesioned rats and hamsters. , 1968, Journal of comparative and physiological psychology.

[48]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[49]  W. R. Klemm,et al.  Physiological and behavioral significance of hippocampal rhythmic, slow activity (“theta rhythm”) , 1976, Progress in Neurobiology.

[50]  I. Izquierdo,et al.  Field potentials in rat hippocampus: Monosynaptic nature and heterosynaptic post-tetanic potentiation , 1968 .

[51]  Brad C. Motter,et al.  Influences of hypothalamic stimulation upon septal and hippocampal electrical activity in the cat , 1976, Brain Research.

[52]  L. Cermak,et al.  Some Analyses of Amnesic Syndromes in Brain-Damaged Patients , 1975 .

[53]  G. Lynch,et al.  Potentiation of excitatory synaptic transmission in the normal and in the reinnervated dentate gyrus of the rat , 1976, Experimental Brain Research.

[54]  T. Teyler,et al.  Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice , 1976, Brain Research.

[55]  James L Olds,et al.  Conditioned responses of hippocampal and other neurons. , 1969, Electroencephalography and clinical neurophysiology.

[56]  P. Best,et al.  Hippocampal unit activity to tonal stimuli during arousal from sleep and in awake rats , 1975, Experimental Neurology.

[57]  P. Andersen,et al.  Two generators of hippocampal theta activity in rabbits , 1975, Brain Research.

[58]  A H Black,et al.  Avoidance training of hippocampal theta waves in flaxedilized dogs and its relation to skeletal movement. , 1970, Journal of comparative and physiological psychology.

[59]  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.

[60]  F. Bloom,et al.  A radioautographic study of the efferent pathways of the nucleus locus coeruleus , 1974, The Journal of comparative neurology.

[61]  H. Karten,et al.  Autoradiographic localisation of α-bungarotoxin-binding sites in the central nervous system , 1975, Nature.

[62]  Frequency analysis of rat hippocampal electrical activity , 1975, Physiology & Behavior.

[63]  R. F. Thompson,et al.  Neuronal substrate of classical conditioning in the hippocampus , 1976, Science.

[64]  W. Spencer,et al.  Penicillin-induced interictal discharges from the cat hippocampus. II. Mechanisms underlying origin and restriction. , 1969, Journal of neurophysiology.

[65]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

[66]  P. Schwartzkroin,et al.  Long-lasting facilitation of a synaptic potential following tetanization in thein vitro hippocampal slice , 1975, Brain Research.

[67]  D. P. Artemenko Laminar analysis of hippocampal potentials evoked by peripheral stimulation , 1970, Neurophysiology.

[68]  J. Phillis,et al.  Acetylcholine sensitivity of hippocampal formation neurons. , 1974, Canadian journal of physiology and pharmacology.

[69]  G L Gerstein,et al.  Single-unit activity in temporal association cortex of the monkey. , 1967, Journal of neurophysiology.

[70]  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.

[71]  A. Rotterdam A discrete formalism for the computation of extracellular potentials , 1973, Kybernetik.

[72]  P. Andersen,et al.  Organization of the hippocampal output , 1973, Experimental Brain Research.

[73]  B. Kaada,et al.  The relation of hippocampal theta activity to arousal, attentive behaviour and somato-motor movements in unrestrained cats , 1975, Brain Research.

[74]  J. Altman,et al.  The hippocampus and behavioral maturation. , 1973, Behavioral biology.

[75]  T. A. Mering,et al.  Functional significance of the hippocampus , 1973 .

[76]  C. Stumpf,et al.  Drug action on the electrical activity of the hippocampus. , 1965, International review of neurobiology.

[77]  P. Maclean,et al.  Hippocampal influence on unit activity of hypothalamus, preoptic region, and basal forebrain in awake, stting squirrel monkeys. , 1973, Journal of neurophysiology.

[78]  E. Kandel,et al.  Hippocampal neuron responses to selective activation of recurrent collaterals of hippocampofugal axons , 1961 .

[79]  C. L. Votaw,et al.  Certain functional and anatomical relations of the cornu ammonis of the macaque monkey. II. Anatomical relations , 1959, The Journal of comparative neurology.

[80]  D. Lindsley,et al.  Hippocampal electrical correlates of free behavior and behavior induced by stimulation of two hypothalamic-hippocampal systems in the cat , 1975, Experimental Neurology.

[81]  J. Eccles Inhibition in Thalamic and Cortical Neurones and its Role in Phasing Neuronal Discharges , 1965, Epilepsia.

[82]  N. Hori,et al.  The correlation between extracellular potassium concentration and hippocampal epileptic activity in vitro , 1976, Brain Research.

[83]  R. Chronister,et al.  Fiberarchitecture of the Hippocampal Formation: Anatomy, Projections, and Structural Significance , 1975 .

[84]  S. Torii Two types of pattern of hippocampal electrical activity induced by stimulation of hypothalamus and surrounding parts of rabbit's brain. , 1961, The Japanese journal of physiology.

[85]  I. Whishaw,et al.  Anterior hypothalamic electrical stimulation and hippocampal EEG in the rat: suppressed EEG, locomotion, self-stimulation and inhibition of shock avoidance. , 1975, Behavioral biology.