The relation of hippocampal theta activity to arousal, attentive behaviour and somato-motor movements in unrestrained cats

EEG recordings of hippocampal theta activity and neocortical activity were correlated with direct observations and photographic recordings of the behaviour of unrestrained cats. The behaviour studied included (1) both spontaneous and induced changes in level of arousal (sleep-wakefulness), (2) different types of orienting activity that occur as the animal is repeatedly exposed to a novel environment, and (3) activities such as walking, drinking, and grooming. With increases in arousal, amount of hippocampal theta activity increased in direct association with extent of pupillary dilatation, degree of eye opening, and extent of neocortical desynchronization. Conversely, with spontaneous or habituation-induced reductions of arousal, amount of hippocampal theta activity became reduced. Maximal hippocampal theta activity was associated with the increased eye movement phase of REM sleep and, during wakefulness, with fixed staring and visual searching behaviour ('tonic' orienting activity). In contrast, hippocampal theta activity was suppressed or attenuated during reflexive head turning ('phasic' orienting behaviour) and other stereotyped movements such as drinking, grooming and undirected locomotor activity unaccompanied by attentive behaviour. These results suggest that theta activity is primarily related to arousal and its control by attentional mechanisms.

[1]  A. Routtenberg Hippocampal correlates of consummatory and observed behavior , 1968 .

[2]  HIPPOCAMPAL ACTIVITY DURING AVOIDANCE BEHAVIOR IN THE RAT. , 1964, Journal of comparative and physiological psychology.

[3]  D. Berlyne,et al.  Novelty, arousal, and the reinforcement of diversive exploration in the rat. , 1966, Journal of comparative and physiological psychology.

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

[5]  W. R. Adey Neurophysiological correlates of information transaction and storage in brain tissue , 1965 .

[6]  G. Karmos,et al.  The hippocampal electrical correlates of the homeostatic regulation of motivation. , 1966, Electroencephalography and clinical neurophysiology.

[7]  B. Frankenhaeuser,et al.  A note on an inhibitory reflex from the nose on the rabbit. , 1949, Acta Physiologica Scandinavica.

[8]  L. Pickenhain,et al.  Hippocampal slow wave activity as a correlate of basic behavioral mechanisms in the rat. , 1967, Progress in brain research.

[9]  F. Bremner Hippocampal electrical activity during classical conditioning. , 1968, Journal of comparative and physiological psychology.

[10]  G. Moruzzi,et al.  Brain stem reticular formation and activation of the EEG. , 1949, Electroencephalography and clinical neurophysiology.

[11]  I. Krekule,et al.  Inter-individual differences in hippocampal theta activity during habituation. , 1970, Electroencephalography and clinical neurophysiology.

[12]  Vanderwolf Ch Limbic-diencephalic mechanisms of voluntary movement. , 1971 .

[13]  J. Brugge,et al.  AN ELECTROGRAPHIC STUDY OF THE HIPPOCAMPUS AND NEOCORTEX IN UNRESTRAINED RATS FOLLOWING SEPTAL LESIONS. , 1965, Electroencephalography and clinical neurophysiology.

[14]  W. R. Adey,et al.  Spectral analysis of low frequency components in the electrical activity of the hippocampus during learning. , 1967, Electroencephalography and clinical neurophysiology.

[15]  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.

[16]  E. John,et al.  ELECTROPHYSIOLOGICAL CORRELATES OF DIFFERENTIAL APPROACH‐AVOIDANCE CONDITIONING IN CATS1 , 1960, The Journal of nervous and mental disease.

[17]  J. Gray,et al.  Medial septal lesions, hippocampal theta rhythm and the control of vibrissal movement in the freely moving rat. , 1971, Electroencephalography and clinical neurophysiology.

[18]  B H Bland,et al.  Electrical stimulation of the hippocampal formation: behavioral and bioelectrical effects. , 1972, Brain research.

[19]  M. Ito,et al.  Hippocampal electrical correlates of self-stimulation in the rat. , 1966, Electroencephalography and clinical neurophysiology.

[20]  W. R. Adey,et al.  THE HIPPOCAMPUS AND THE ORIENTING REFLEX. , 1965, Experimental neurology.

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

[22]  J. Gottfried,et al.  Hippocampal theta activity and response inhibition. , 1970, Electroencephalography and clinical neurophysiology.

[23]  J. Lát THE SPONTANEOUS EXPLORATORY REACTIONS AS A TOOL FOR PSYCHOPHARMACOLOGICAL STUDIES. A CONTRIBUTION TOWARDS A THEORY OF CONTRADICTORY RESULTS IN PSYCHOPHARMACOLOGY , 1965 .

[24]  W. R. Adey,et al.  Subthalamic lesions. Effects on learned behavior and correlated hippocampal and subcortical slow-wave activity. , 1962, Archives of neurology.

[25]  D. E. Berlyne,et al.  CHAPTER 7 – The Reward-Value of Indifferent Stimulation1 , 1969 .

[26]  K. Konrad,et al.  Effect of novel stimuli on cats reared in a restricted environment. , 1970, Journal of comparative and physiological psychology.

[27]  Z. Hrůza The relationship of the individual differences in the regulation of food intake, growth and excitability of the central nervous system. , 1956 .

[28]  James L Olds,et al.  Units during habituation, discrimination learning, and extinction. , 1970, Electroencephalography and clinical neurophysiology.

[29]  F. D. da Silva,et al.  Hippocampal frequency shifts in different behavioural situations. , 1971, Brain research.

[30]  D. Berlyne,et al.  Arousal and Reinforcement , 1967 .

[31]  EFFECTS OF SMALL HIPPOCAMPAL LESIONS ON LOCALLY RECORDED POTENTIALS AND ON BEHAVIOR PERFORMANCE IN THE CAT. , 1964, Experimental neurology.

[32]  J. Sprague,et al.  Progress in physiological psychology , 1966 .

[33]  J. Winson,et al.  Interspecies differences in the occurrence of theta. , 1972, Behavioral biology.

[34]  R B MALMO,et al.  Activation: a neuropsychological dimension. , 1959, Rassegna giuliana di medicina.

[35]  H. Ursin,et al.  Habituation to electrical stimulation of the brain in unanesthetized cats. , 1967, Electroencephalography and clinical neurophysiology.

[36]  C. H. Vanderwolf,et al.  Hippocampal activity, behavior, self-stimulation, and heart rate during electrical stimulation of the lateral hypothalamus. , 1972, Journal of comparative and physiological psychology.

[37]  W. R. Adey,et al.  Electrical activity of the entorhinal cortex during conditioned behavior. , 1960, The American journal of physiology.

[38]  C. Stumpf THE FAST COMPONENT IN THE ELECTRICAL ACTIVITY OF RABBIT'S HIPPOCAMPUS. , 1965, Electroencephalography and clinical neurophysiology.

[39]  W. R. Adey,et al.  Hippocampal slow waves. Distribution and phase relationships in the course of approach learning. , 1960, Archives of neurology.

[40]  P. Andersen Inhibitory reflexes elicited from the trigeminal and olfactory nerves in rabbits. , 1954, Acta physiologica Scandinavica.

[41]  W. R. Adey,et al.  Electroencephalographic correlates of learning in subcortical and cortical structures. , 1967, Electroencephalography and clinical neurophysiology.

[42]  D. Hebb Drives and the C.N.S. (conceptual nervous system). , 1955, Psychological review.

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

[44]  T. L. Bennett Hippocampal EEG correlates of behavior. , 1970, Electroencephalography and clinical neurophysiology.

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

[46]  W. R. Adey,et al.  Application of phase detection and averaging techniques in computer analysis of EEG records in the cat. , 1963, Experimental neurology.

[47]  B. Kaada,et al.  Failure to modulate autonomic reflex discharge by hippocampal stimulation in rabbits. , 1971, Physiology & behavior.

[48]  I. Whishaw Hippocampal electroencephalographic activity in the Mongolian gerbil during natural behaviours and wheel running and in the rat during wheel running and conditioned immobility. , 1972, Canadian journal of psychology.

[49]  R. Sainsbury,et al.  Hippocampal activity during natural behavior in the guinea pig. , 1970, Physiology & behavior.

[50]  I Q Whishaw,et al.  Hippocampal EEG and behavior: effects of variation in body temperature and relation of EEG to vibrissae movement, swimming and shivering. , 1971, Physiology & behavior.

[51]  K. Pribram,et al.  Limbic lesions and error reduction. , 1969, Journal of comparative and physiological psychology.

[52]  B. Kaada,et al.  Differential effects of hippocampal lesions on maze and passive avoidance learning in rats , 1964 .

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

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