Diencephalic and hippocampal mechanisms of motor activity in the rat: Effects of posterior hypothalamic stimulation on behavior and hippocampal slow wave activity

doi:10.1016/0006-8993(72)90275-2

Brain Research

Volume 43, Issue 1, 11 August 1972, Pages 67-88

https://doi.org/10.1016/0006-8993(72)90275-2 Get rights and content

Summary

Slow wave activity was recorded from the hippocampus in chronically prepared rats. During spontaneous or learned behavior, rhythmical slow activity (RSA) accompanied walking, rearing, climbing, manipulation of objects with the forelimbs, isolated movements of the head or one limb and changes in posture (voluntary movement) but did not accompany alert immobility, licking, chewing, face-washing, or scratching (more automatic behavior). During stimulation of the hypothalamus similar behavior-EEG relations were observed. Walking, running, jumping, and isolated head movements were always accompanied by RSA, but this waveform was absent during alert immobility, chewing, face washing, piloerection or chattering of the teeth.

Stimulation of the dorsomedial posterior hypothalamus was especially effective in the elicitation of RSA in the hippocampus and also consistently produced head movement, running, or jumping when administered in conscious animals. Sites in the dorsomedial-posterior hypothalamus would also support self-stimulation behavior. Increases in the voltage of posterior hypothalamic stimulation produced increases in the frequency of the RSA during the first few seconds of stimulation, and a corresponding increase in running speed or in the force with which jumping was initiated. Relations between behavior and hippocampal activity were the same during tests of learning (active and passive avoidance) and during spontaneous behavior (e.g., exploration). It is suggested that an ascending hypothalamo-hippocampal mechanism plays a role in the control of voluntary movement.

References (37)

KawamuraH. et al.
Hippocampal slow (‘arousal’) wave activation in the rostral midbrain transected rat
Electroenceph. clin. Neurophysiol.
(1968)
KramisR.C. et al.
Rewarding brain stimulation, hippocampal activity, and foot-stomping in the gerbil
Physiol. Behav.
(1969)
McGintyD.J.
Somnolence, recovery and hyposomnia following ventromedial diencephalic lesions in the rat
Electroenceph. clin. Neurophysiol.
(1969)
PaxinosG. et al.
Rewarding intracranial stimulation, movement, and the hippocampal theta rhythm
Physiol. Behav.
(1970)
SainsburyR.S.
Hippocampal activity during natural behavior in the guinea pig
Physiol. Behav.
(1970)
StumpfCh.
The fast component in the electrical activity of the rabbits' hippocampus
Electroenceph. clin. Neurophysiol.
(1965)
VanderwolfC.H.
Hippocampal electrical activity and voluntary movement in the rat
Electroenceph. clin. Neurophysiol.
(1969)
WhishawI.Q. et al.
Hippocampal EEG and behavior: Effects of variation in body temperature and relation of EEG to vibrissae movement, swimming and shivering
Physiol. Behav.
(1971)
YoshiiN. et al.
Studies on the neural basis of behavior by continuous frequency analysis of EEG
BlackA.H. et al.
Avoidance training of hippocampal theta waves in Flaxedilized dogs and its relation to skeletal movement
J. comp. physiol. Psychol.
(1970)

CampbellB.A. et al.

Electrical and behavioral effects of different types of shock stimuli on the rat

J. comp. physiol. Psychol.

(1958)

DaltonA. et al.

Hippocampal electrical activity during the operant conditioning of movement and refraining from movement

Commun. Behav. Biol.

(1968)

GerbenM.J.

Running elicited by hypothalamic stimulation

Psychon. Sci.

(1968)

GerbenM.J.

Elicited locomotor behavior during hypothalamic self-stimulation

Commun. Behav. Biol.

(1969)

GranitR. et al.

Influence of stimulation of central nervous structures on muscle spindles in cat

Acta physiol. scand.

(1952)

GreenJ.D. et al.

Hippocampal electrical activity in arousal

J. Neurophysiol.

(1954)

GreenJ.D. et al.

Rabbit EEG ‘theta rhythm’: its anatomical source and relation to activity in single neurons

J. Neurophysiol.

(1960)

GriffithsE. et al.

An apparatus for detecting and monitoring movement

Amer. J. Psychol.

(1967)

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Our results indicate that the triceps, a muscle involved in locomotion, can be activated by direct electrical stimulation of the CA1 region in the hippocampus. Electrical stimulation in the posterior hypothalamus produce theta-like activity and locomotion initiation (Bland and Vanderwolf, 1972; Slawinska and Kasicki, 1995; Oddie et al., 1996), both the hippocampus and the posterior hypothalamus pertain to the sensory-motor integration model altogether with the medial septum and other structures (Bland, 2009). An injury in the posterior hypothalamus, produces akinesia and a loss of the atropine sensitive theta wave (Robinson and Whishaw, 1974).
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^*: Present address: Institute of Neurophysiology, University of Oslo, Karl Johans Gt. 47, Oslo 1, Norway.

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Diencephalic and hippocampal mechanisms of motor activity in the rat: Effects of posterior hypothalamic stimulation on behavior and hippocampal slow wave activity

Summary

Electroenceph. clin. Neurophysiol.

Physiol. Behav.

Electroenceph. clin. Neurophysiol.

Physiol. Behav.

Physiol. Behav.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Physiol. Behav.

Avoidance training of hippocampal theta waves in Flaxedilized dogs and its relation to skeletal movement

J. comp. physiol. Psychol.

Electrical and behavioral effects of different types of shock stimuli on the rat

J. comp. physiol. Psychol.

Hippocampal electrical activity during the operant conditioning of movement and refraining from movement

Commun. Behav. Biol.

Running elicited by hypothalamic stimulation

Psychon. Sci.

Elicited locomotor behavior during hypothalamic self-stimulation

Commun. Behav. Biol.

Influence of stimulation of central nervous structures on muscle spindles in cat

Acta physiol. scand.

Hippocampal electrical activity in arousal

J. Neurophysiol.

Rabbit EEG ‘theta rhythm’: its anatomical source and relation to activity in single neurons

J. Neurophysiol.

An apparatus for detecting and monitoring movement

Amer. J. Psychol.