Journal of Comparative and Physiological Psychology 1975, Vol. 88, No. 1, 324-328

RELATIONSHIP BETWEEN HIPPOCAMPAL THETA ACTIVITY AND RUNNING SPEED IN THE RAT1 WILLARD L. McFARLAND 2 Armed Forces Radiobiology Research Institute, Bethesda, Maryland HERMAN TEITELBAUM AND ELIZABETH K. HEDGES University of Maryland The frequency of occurrence and amplitude of hippocampal theta waves induced by forced locomotion is proportional to speed of movement on a treadmill. Although induction of hippocampal theta waves is related to the initiation of movement, it is not dependent upon proprioceptive feedback because it persists in the resting animal after a bout of running. It is possible to obtain cortical theta waves in the absence of hippocampal theta activity.

A 6-8 Hz. (theta) rhythm often becomes a prominent feature of the bioelectric activity of the hippocampus in a variety of species. Conjecture as to the conditions under which this theta activity arises and its biological significance includes hypotheses that it is involved in learning and memory consolidation (Elazar & Adey, 1967), orienting responses (Bennett & Gottfried, 1970; Grastyan, Lissak, Madarasz, & Donhoffer, 1959), or movement (Black, Young, & Batenchuk, 1970; Dalton & Black, 1968; Teitelbaum & McFarland, 1971; Vanderwolf, 1969,1971; Vanderwolf & Heron, 1964; Whishaw, 1972; Whishaw & Vanderwolf, 1973). The latter hypothesis is especially interesting because movement of the experimental subject has not been controlled in experiments designed to examine other hypotheses concerned with the significance of hippocampal theta activity (Elazar & Adey, 1967; Grastyan et al., 1959). Previous work in this laboratory (Teitelbaum & McFarland, 1971) has shown that hippocampal bioelectric activity becomes synchronized around a 7-Hz. peak and its amplitude increases relative to that during inactive 1 This report is based in part on a dissertation submitted by Elizabeth K. Hedges in partial fulfillment of the requirements for the MA degree at the University of Maryland. This research was supported by Office of Naval Research Contract NR 201-037. 2 Requests for reprints should be sent to W. L. McFarland, Division of Research Grants, National Institutes of Health, Westwood Building, Bethesda, Maryland 20014.

periods in rats trained to increase their activity levels. To establish whether it was the particular conditioning procedure or the movement itself that led to the induction of theta waves in the hippocampus of our trained rats, it was necessary to induce changes in locomotion by means other than operant conditioning based upon positive reinforcement. In the present experiment, rats are forced to run at varying speeds in a treadmill. In this manner the relationship between speed of movement and changes in hippocampal bioelectric pattern can be determined. METHOD AND MATERIALS Six male Sprague-Dawley rats, weighing250-370 gm., were anesthetized with sodium pentobarbital (50 mg/kg) and placed in a Kopf stereotaxic instrument. With the top of the tooth bar set 2.5 mm. below ear-bar zero, the skull surface lay in a horizontal plane. The coordinates for the hippocampal electrodes were 2.0 mm. behind bregma, 2.0 mm. lateral, and 4.5 mm. below the skull surface. These coordinates resulted in placement of recording tips in the vicinity of the pyramidal cell layer of the CAt and CA2 fields of the dorsal hippocampus (see Teitelbaum & McFarland, 1971). Miniature gold-plated "poke-home" (Amphenol Co.) pins placed bilaterally upon the occipital region served as cortical recording electrodes. After allowing 1 wk. for recovery from surgery, EEG recording leads were attached directly to the poke-home pins, and the rats placed in the treadmill. The bioelectric signals were amplified differentially by Tektronix FM122 units with a bandpass setting of .2-50 Hz. and recorded on both a dynograph paper chart recorder and on a 7-channel Ampex HP-300 tape recorder. A graphic time code

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HIPPOCAMPAL THETA AND RUNNING was also recorded on both instruments. Later, the signals from both cortex and hippocampus were fed through a Krohn-Hite 3550-R filter set at band passes of 6-8 Hz. or 10-12 Hz. At the 6-8 Hz. setting, half power points were 5.4 Hz. and 9.1 Hz.; at the 10-12 Hz. setting, half power points were 8.5 Hz. and 14.3 Hz. The filter output was then passed through a Schmitt trigger set to fire at a predetermined voltage level. The trigger outputs were recorded on a cumulative recorder. The threshold firing level of the Schmitt trigger was different for cortical and hippocampal signals due to differences in signal amplitude, but was always the same for a given structure in a given rat. The rats were initially placed in the treadmill with the motor off, and a baseline (Bl) EEG obtained. Next, the rat was placed on a plastic sheet suspended above the treadmill belt, and the motor turned on. This served as a control for possible artifacts generated by the motor. The plastic sheet was then removed, and the rat was forced to run at a variety of speeds ranging 1-22 cm/sec for approximately 5 min. at each speed. The order of the speeds was counterbalanced from day to day. A second baseline (B2) was obtained with the motor off at the end ot each day's running session. A minimum of 3 days of running sessions was obtained from each rat.

RESULTS As soon as the treadmill was turned on, the hippocampal EEG showed marked changes. The amplitude of the EEG increased, and the tracing changed from asynchronous activity to activity synchronized at about 7 Hz. The cortex did not show such systematic changes in frequency or amplitude. This phenomenon is clearly illustrated in Figure 1 in which a comparison is made of cortical and hippocampal recordings obtained from a rat at rest (Bl and B2) and while running at various speeds. In the hippocampal tracings, note that there is little change from baseline to motor conditions. The signals are of variable amplitude, and there is little theta present. At a speed of 1 cm/sec, theta activity increases, and there is greater synchronization of the waveforms at the theta frequencies. Both synchronization and amplitude steadily increase to reach their maximum at 22 cm/sec treadmill

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W. L. McFARLAND, H. TEITELBAUM, AND E. K. HEDGES CUMULATIVE W A V E COUNTS RAT 195

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FIGURE 2. Top: A comparison of cumulative wave counts in 2 distinct regions of the hippocampal frequency spectrum as a function of forced movement on a treadmill. (As the subject is forced to run at progressively faster speeds, there is a greater change in the hippocampal EEG in the 6-8 Hz. band than in the 10-12 Hz. band.) Bottom: Cumulative wave counts in the 6-8 Hz. band of the cortical EEG frequency spectrum as a function of forced movement on a treadmill. (Unlike the hippocampal EEG changes shown above, there is no systematic change in cortical EEG in the theta band with forced movement in a treadmill.)

speed. In contrast, the cortical tracing shows only a slight amplitude increase at 15 and 22 cm/sec, and there is no noticeable synchronization at theta frequencies at any speed. The cortical and hippocampal recordings shown in Figure 3 were filtered through narrow "windows" of a Krohn-Hite bandpass filter. The output of the filter varies as a function of the EEG voltage between, the given frequency settings. The filtered EEG signals of rats running at different treadmill speeds were then fed into a voltage sensor (Schmitt trigger). Pulses from the trigger

actuated a relay in a cumulative recorder that provided a graphic record of changes in output of the filter set at frequency bands within (6-8 Hz.) and outside (10-12 Hz.) the theta band. The results of this analysis are shown in Figure 2. The conditions Bl and B2 refer to baseline conditions when the animal was sitting quietly. In the "motor" condition, the motor was turned on, but the treadmill was disengaged to control for possible electrical artifacts. In Figure 2 (top) the results of the analysis of the hippocampal EEG are presented. A comparison is made of changes in the 6-8 Hz. band (theta) and the 10-12 Hz. band (nontheta) as a function of different experimental conditions. It is quite clear that there is a greater change of activity in the 6-8 Hz. band than in the 10-12 Hz. band when the rat is forced to run in the treadmill. Furthermore, the rate of change is proportional to the speed the animal is forced to maintain. This clear-cut relationship is not seen in the analysis of the cortical tracings (Figure 2, bottom). Here we see no consistent changes in either frequency band as a function of running speed. The systematic change shown in the theta component of the hippocampal tracing was seen in every animal. However, no consistent frequency change was found in the cortex. At the highest speeds, there was an increase in signal amplitude, but this was not specific to either frequency band. Although there was a very good correlation of the induction of theta with the onset of movement, hippocampal theta did not stop immediately with cessation of movement. This is illustrated in Figure 3. Occasionally in this laboratory, we have been able to record from cortical sites tracings that look identical to hippocampal theta. Some investigators (Yamaguchi, Yoshii, Miyamoto, & Itoigawa, 1967) have noted this and have explained it on the basis of volume conduction from hippocampus. Recordings from Animal 181, shown in Figure 3, have a direct bearing on this question. At the top of the figure are records obtained while the rat is running at a very fast speed. In the middle are records taken right after the cessation of running, and the lower traces

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HIPPOCAMPAL THETA AND RUNNING CORT

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are taken 6 min. after the end of running. in hippocampal theta activity in curarized Note the differences in synchrony and am- dogs. The need for adequate movement conplitude of the hippocampal traces in the 3 conditions. Theta waves are most prominent trols in experiments relating altered hippoin Condition A and only sporadically present campal bioelectric patterns to cognitive or in Condition C. In contrast, note that theta mnemonic processes has been emphasized waves are continuously present in the cortex by Vanderwolf (1971). The present findings even in Condition C when they are less provide additional evidence of the sensitivity evident in the hippocampus. This can only of neuron pools in the dorsal hippocampus mean that there are independent sources for of the rat to altered patterns of locomotor the generation of theta waves at these loci. activity. On the basis of work reported here and It is quite possible that other hippocampal loci share common theta generators with elsewhere (Teitelbaum & McFarland, 1971) and work by others (Vanderwolf & Heron, cortical loci. 1964; Whishaw, 1972), we conclude that DISCUSSION movement-induced changes in hippocampal bioelectric activity are independent of the By demonstrating a relationship between motive state "releasing" the loccmotor rebodily activity and generation of hipposponse. campal theta waves, these data clearly REFERENCES support our previous (1971) findings and those of Vanderwolf and Heron (1964), Bennett, T. L., & Gottfried, J. Hippocampal theta Vanderwolf (1969, 1971), Whishaw (1972), activity and response inhibition. Electroencephalography and Clinical Neurophysiology, 1970, and Whishaw and Vanderwolf (1973). In 29, 196-200. addition, these results extend the previous Black, A. H., Young, G. A., & Batenchuk, C. findings by showing a monotonic relationAvoidance training of hippocampal theta waves ship between amount of hippocampal theta in flaxedilized dogs and its relation to skeletal movement. Journal oj Comparative and Physiactivity and speed of movement. The data ological Psychology, 1970, 70, 15-24. showing that hippocampal theta waves perDalton, A., & Black, A. H. Hippocampal electrical sist for some time after the cessation of activity during the operant conditioning of running suggests that increased propriomovement and refrain-from movement. Comceptive inflow from active muscles is not a munications in Behavioral Biology, Ft. A, 1968, 2, 267-273. necessary condition for the occurrence of hippocampal theta waves as suggested by Elazar, Z., & Adey, W. R. Spectral analysis of low frequency components in the electrical activity Klemm (1970). Black et al. (1970) demonof the hippocampus during learning. Electroenstrated this dissociation in a different mancephalography and Clinical Neurophysiology, ner by successfully conditioning an increase 1967, 23, 225-240.

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Grastyan, E., Lissak, K., Madarasz, I., & Donhoffer, H. Hippocampal electrical activity during the development of conditioned reflexes. Electroencephalography and Clinical Neurophysiology, 1959,11, 409-430. Klemni, W. R. Correlation of hippocampal theta rhythm, muscle activity, and brain stem reticular formation activity. Communications in Behavioral Biology, 1970, 5,147-151. Teitelbaum, H., & McFarland, W. L. Power spectral shifts in the hippocampal EEG associated with conditioned locomotion in the rat. Physiology and Behavior, 1971, 7, 545-549. Vanderwolf, C. H. Hippocampal electrical activity and volutary movement in the rat. Electroencephalography and Clinical Neurophysiology, 1969, 26, 407-418. Vanderwolf, C. H. Limbic-diencephalic mechanisms of voluntary movement. Psychological Review, 1971,78,83-113. Vanderwolf, C. H., & Heron, W. Electroencephalo-

graphic waves with voluntary movement. Archives oj Neurology, 1964,11, 379-384. Whishaw, I. Q. Hippocampal electroencephalographic activity in the mongolian gerbil during natural behaviours and wheel running and in the rat during wheel running and conditioned immobility. Canadian Journal of Psychology, 1972, 26,219-239. Whishaw, I. Q., & Vanderwolf, C. H. Hippocampal EEG and behavior: changes in amplitude and frequency of RSA (theta rhythm) asociated with spontaneous and learned movement patterns in rats and cats. Journal oj Behavioral Biology, 1973, 8, 461-484. Yamaguchi, Y., Yoshii, N., Miyamoto, K., & Itoigawa, N. A study on the invasive hippoeampal theta waves to the cortex. In W. R. Adey & T. Tokizane (Eds.), Progress in brain research, Amsterdam: Elsevier. 1967. (Received October 10,1973)

Relationship between hippocampal theta activity and running speed in the rat.

The frequency of occurrence and amplitude of hippocampal theta waves induced by forced locomotion is proportional to speed of movement on a treadmill...
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