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Habituation of the orienting response elicited by stimulation of the caudate nucleus in the cat
Newopsychologia,
1969, Vol. 7, pp. 313 to 318. Pergamon Pmss. Printed in England
HABITUATION OF THE ORIENTING RESPONSE ELICITED BY STIMULATION OF THE CAUDATE NUCLEUS IN THE CAT HOLCEKURSIN, HKKAN SUNDBERGand STEVENMENAKER Institute of Physiology, University of Bergen, Norway (Received 6 January 1969) Abstract-High frequency (lOO/sec) electrical stimulation of eight points in the head of the caudate nucleus in six unanesthetized, freely moving cats yielded an orienting response from all points. The behavior observed was indistinguishable from the orienting response elicited by novel, acoustic stimulation and by electrical stimulation of the amygdala, parts of cortex, and the mesencephalic reticular formation. The cats habituated to the caudate stimulation just as cats habituate to non-signal, peripheral sensory events. The same has previously been found for stimulation of amygdala and cortex, while no habituation is observed to stimulation of the mesencephalic reticular formation.
As EARLY as 1875 DANILEWSKI[I] reported that electrical stimulation of the caudate nucleus resulted in slowing of breathing and a cessation of spontaneous movements. Later research [2, 31 also describes inhibitory functions for this nucleus. KAADA[4] described two general types of inhibitory phenomena elicited by electrical stimulation, a short lasting arrest with no loss of muscle tone, and a long lasting inhibition with loss of muscle tone. In later work, KAADAand collaborators found that the short lasting arrest observed during anesthesia is a part of the orienting response. When these “arrest” zones are stimulated in freely moving cats, the whole orienting response is seen; there is initial arrest of ongoing activity followed by orienting movements, behavioral arousal and electroencephalographic desynchronization [5-71. The present report deals with two questions: Is the behavior response elicited by electrical stimulation of the caudate nucleus of a broad inhibitory nature, or is the response identical to the orienting responses we have observed from the stimulation of other structures? If orienting responses are elicited, are they subject to habituation in the same way as those elicited by stimulation of the other arrest areas [8], or do associated inhibitory phenomena interfere with gradual disappearance of the orienting response? MATERIALS
AND METHODS
A total of 8 electrodes in 6 cats constitute the material. Electrodes were implanted during anesthesia by the ordinary stereotaxic procedure. Electrodes were 0.18 mm thin platinum wires covered by Teflon except for 1 mm at the tip, protruding into the brain tissue through a stainless steel catheter of 0.6 mm bore. This shielding served as ground for the unipolar stimulation. The animal was stimulated while freely moving in an observation chamber (45 x 55 x 145 cm) surrounded by a one-way mirror on one side, and conventional mirrors on the other three sides. The cats were stimulated by a radiocontrolled stimulator [9]. A “stimoceiver” carried by the cat weighed 14 g including battery. The stimoceivers were found ,to work reliably, producing constant current rectangular pulses. Pulse width, 313
HOLGER URSIN, H~KAN SUNDBEROand STEVENMENAKER
314
frequency and amplitude could be controlled from the radio transmitter. The frequency used was lOO/sec of 1 msec duration. The observation chamber, two observers, and the radio transmitter were placed inside an electrically shielded and sound-attenuated room. The intensity of the orienting response was evaluated by a scoring method described previously. Briefly, it consisted of four categories of behavior (see Table 1, modified from ROELOFFSet al. [lo]). The level of arousal was evaluated just before stimulus onset, and a second score was given for the behavior during and immediately after the stimulation. The difference between these two scores has been used as an indicator for the arousal effect of stimulation. Table 1. Scoring schedule
Points
Head
Eye-lids
Pars
6
Posture Running
5
Searching
Walking
4
Turning
Open
3
Lifted
Half open
2
Quiet
Membrana contracted
1
Laid down
Closed
Standing
nict.
Moving
Sitting
Quiet
Lying on belly
Curled up or lying on side
The cats had not been used for other experiments before the operation. At least 48 hours after screening the effects from the various electrode sites, avoiding unnecessary stimulation, habituation sessions were run for all electrode sites yielding clear-cut orienting responses. Stimulation intensity was chosen separately for each site as the lowest intensity giving a pre- and post-stimulatoty difference of at least 3 points in the behavior score. Intertrial intervals varied from 30 set to several minutes, a stimulus was never given unless the cat was quiet (behavior score less than 9). Habituation was said to occur when the cat, for three trials in a row, did not show more than 0.5 in the difference between the pre-and post-stimulation score. Dishabituation was then produced by introducing other arousal stimuli, and the number of trials necessary to produce rehabituation was tested for most electrodes. At the end of the experiment the animals were killed, the brains perfused and the electrode sites identified histologically in N&l-stained material.
RESULTS Caudate orienting responses
Electrical stimulation of the caudate nucleus elicited highly predictable changes in behavior. Any ongoing activity was stopped immediately at the stimulus onset, once threshold had been reached (“arrest”). Then the eyes were opened, the ears were moved forward, and the head was lifted and turned to the side opposite of that stimulated. This head movement was often slow, stepwise, and oscillating, and was referred to as “searching” in the scoring categories. The cat often sat up and moved around at higher intensities. The time course depended on the stimulation intensity. The response was adequately described by the scoring categories shown in Table 1, and is indistinguishable from the response (“orienting response”) seen when a cat is subjected to any novel stimulus. Other responses
One additional electrode, situated dorsally in the left caudate nucleus, yielded no observable orienting response. During stimulation, simple motor movements such as turning around the body axis, chewing, and mouth opening were observed. Following
WI3 OBIENTINQ BESPONSE ELICITBD BY STIMULATION OF THB CAUDATE NUCLEUS IN THE CAT
315
stimulation, the cat seemed alerted but no clearcut orienting response was observed. In addition to orienting responses at low current intensity for other sites, a stronger stimulation sometimes led to after-discharges and, occasionally, to full fledged tonic-clonic fits. Habituation to stimulation of the caudate nucleus
Repeated stimulation of the caudate nucleus invariably led to gradual disappearance of the orienting behavior (Fig. 1). A declining slope followed the waxing and waning pattern described as occurring with external stimuli and with electrical stimulation of the amygdala and the cortex [8]. A 15
I
(poinI8)
I
10 t
s I _
J
I .A
1”
I
,
I
I
13
ao
2,
._
__
Stim. no
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Stim. m
sum. no
FIN. 1. Habituation to electrical stimulation of three points (A, B and C) in the caudate nucleus. Open circle: level of arousal before stimulation; open triangle: maximum intensity of orienting response during or immediately following the stimulation; filled circle: no orienting behavior to stimulation. Dishabituation indicated by stippled line. A drop in base line was sometimes observed (A), but this was not a necessary condition for habituation to occur (B). When very few trials were necessary to reach habituation, dishabituation sometimes was difficult to obtain without prolonging the inter-trial interval, or using very intense dishabituating stimuli (C).
The number of trials (Fig. 2) required for habituation of the caudate sites was very close to that required for the amygdala sites, and slightly lower than the level observed for cortical stimulation sites [8].
316
HOLGER URSIN,H~KANSUNDBERG
and STEVENMENAKER
FIG. 2. Frontal sections. Localization of points stimulated indicated by circles, the number inside the circle indicates number of stimulus presentations necessary to reach habituation. A and B, present material; C previously published material [8]. CA, anterior commisure; CAUD, caudate nucleus; CC, corpus callosum; CL, internal capsule; CL, claustrum; DB, diagonal band; Fx, fornix; NA, accumbens; Put, putamen; S, septum; Th, thalamus; V, ventricle.
Dishabituation
When the habituation criteria had been reached the response to stimulation of the caudate nucleus returned again when arousal was produced by some other stimulus, such as knocking on the observation cage. This phenomenon, “dishabituation”, is also illustrated in Fig. 1. When habituation then was again produced by repeating the stimulation, fewer trials were required than for the original habituation. Changing the stimulus parameters also had the same effect. The dishabituating effect did not seem to depend on the kind of stimulus used. These findings are similar to the findings for cortical and amygdala stimulation. Localization
The placement of the electrode sites is shown in Fig. 2. No differential localization of function within the caudate nucleus was observed in the present material. Intecference with ongoing eating
Stimulation of caudate sites in 3 cats during eating showed no evidence of facilitation or inhibition of food intake except for the arrest associated with the orienting response. Consequently, this incidental inhibition of eating disappeared as habituation to the caudate stimulation took place. The same type of interference, limited to arrest and responsecompetition with the orienting response, was seen in four cats where caudate stimulation was given during performance of a learned food-approach response in a Wisconsin General Test Apparatus. DISCUSSION Several authors have pointed out that the behavioral effects observed with stimulation of the caudate nucleus depend on the frequency used [2, 111. Low frequency stimulation in this area, as in many other areas of the brain, elicits a variety of “inhibitory” and sleeplike phenomena that will not be discussed here. In this paper, we are only concerned with the effects of high frequency stimulation of the caudate.
THE ORIJMTING RESPONSE ELICITED BY
STIMULATION OFTHE
CAUDATB NUCLEUS IN THE CAT
317
Contralateral head-turning and circling have been described by most reports on the effects of caudate nucleus stimulation in the freely moving cat. In fact, LAURSEN[12] claimed that these were the only “motor” responses of caudate origin. LAUR~ENfurther stated that the cats looked as if they were searching for something, and he interpreted this response as a complex behavioral manifestation rather than a stereotyped movement. It is our conclusion that this response, observed by most authors with high frequency stimulation, is the same behavior that we have called the orienting response. This has also been suggested by GALEANOet trl. [13]. This response is similar to that elicited by stimulation of the amygdala, the cortex or the mesencephalic reticular formation. In our experience, it is also indistinguishable from the orienting response observed when a novel sound is presented to a cat. It is impossible for us to tell from the observed behavior whether a given orienting response is being elicited by external stimulation or brain stimulation. In none of the electrode sites studied was there any evidence of “inhibitory” phenomena such as eye closure, lying down, or other evidence of sleep or “de-arousal”. The only “inhibitory” phenomena observed were the arrest response that is a part of the orienting response, and the habituation to the stimulation. In other words, there was no additional “inhibition” to the caudate response as compared to the orienting response elicited by external sound or electrical stimulation in the amygdala or over the lateral or supra-sylvian gyrus [81. The gradual decrease of the orienting responses to caudate stimulation is considered to be habituation since the response re-occurred when arousal was produced by some other stimulus. This phenomenon is called “dishabituation”, and is commonly regarded as a necessary condition for concluding that habituation was present [14]. It should be kept in mind that the present habituation concept is limited to decrements in the orienting response, and is not used indiscriminately for any or all response decrements [15]. The presence of dishabituation is a strong argument against interpretations of the response decrement as being due to such artifactual things as polarization of the electrode or damage to the nervous tissue by electrolytical effects. The orienting response elicited by brain stimulation and showing the habituation phenomenon, should not, in our opinion, be interpreted as a motor response elicited from “arousal areas”. The orienting response is the fixed action pattern of any cat to any novel stimulus. Any experience the brain is not “set” to expect will elicit this response. Therefore, it is to be expected that this response will be elicited by stimulation of many different types of functional systems within the brain. There is, therefore, no serious discrepancy between the demonstration of organization within the caudate nucleus discussed by DIVAC[16] and our lack of finding any localization. The experience elicited by caudate stimulation seems to be treated in the same way as adequate sensory stimulation since the response shows the habituation phenomenon. In other words, the brain may identify such stimulations as “non-signals” and stops reacting to them. By contrast, stimulation of the mesencephalic reticular formation does not habituate [8]. In this latter case, therefore, it is most likely that one is dealing with an arousal motor. Still a third way of producing arousal by stimulation of the brain is to interfere with the systems involved in motivational and emotional responses. This has been suggested as a separate arousal system by ROL’TTJZN~ERG [17], and is probably the way arousal and orienting behavior is elicited when the electrodes are close to the pericommisural parts of the septal region (Fig. 2C).
318
HOLGERURSIN,H&CAN SUNDBERG and STEVENMENAKER
REFERENCES 1. DANILEWSKY,B., JR. Experimentelle Beitrlge zur Physiologie des Gehirns. Ppiigers Arch. ges. Physiol. 11, 128-138, 1875. 2. BUCHWALD,N. A., WYERS,E. J., LAUPRECHT,C. W. and HEUSER, G. The “caudate-spindle”. IV. A behavioral index of caudate-induced inhibition. Electroenceph. ctin. Neurophysiol. 13, 531-537, 1961. 3. MET~LER,F. A., ADES, H. W., LIPMAN,E. and CULLER,E. A. The extrapyramidal system. An experimental demonstration of function. A.M.A. Archs. Neurof. Psychiut. 41,984-995, 1939. 4. KAADA, B. R. Somato-motor, autonomic and electrocorticographic responses of “rhinencephalic” and other structures in primates. cat and dog. Acta uhvsiol. scund. 24 (suo~l. 83). l-285. 1951. 5. FANGEL,C. and K~ADA, B. k. Behavior-“attentibl;” and fear induced by co&al stimulation in the cat. Electroenceph. clin. Neurophysiol. 12, 575-588, 1960. 6. KAADA, B. R. and JOHANNESSEN, N. B. Generalized electrocortical activation by cortical stimulation in the cat. Electroenceph. chin. Neurophysiol. 12, 567-573, 1960. 7. URSIN, H. and KAADA, B. R. Functional localization within the amygdaloid complex in the cat. Electroenceph. clin. Neurophysiol. 12, l-20, 1960. 8. URSIN, H., WESTER, K. and URSIN, R. Habituation to electrical stimulation of the brain in unanesthetized cats. Electroenceph. clin. Neurophysiol. 23, 4149, 1967. 9. DELGALIO, J. M. R. Aggressive behavior evoked by radio stimulation in monkey colonies. Am. ZooI. 6, 669-681, 1966. 10. ROELOFS,G. A., VANDENHOOFDAKKER,R. H. and PRECHTL,H. F. R. Sleep effects of subliminal brain stimulation in cats. Expl Neural. 8, 84-92, 1963. 11. MCLENNAN, H., EMMONS,P. R. and PLUMMER,P. M. Some behavioral effects of stimulation of the caudate nucleus in unrestrained cats. Can. J. Physiol. Pharmacol. 42, 329-339, 1964. 12. LAURSEN,A. M. Movements evoked from the region of the caudate nucleus in cats. Actu physiol. stand. 54, 175-184, 1962. J. A. Conditioning of subcortical telencephalic stimula13. GALEANO,C., ROIG, J. A. and SOMMER-SMITH, tion effects. Electroenceph. clin. Neurophysiol. 17, 281-293, 1964. 14. SOKOLOV,Y. N. Perception and the Conditioned Refi’ex. Pergamon Press, Oxford, 1963. 15. THOMPSON,R. F. and SPENCER,W. A. Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73, 16-43, 1966. 16. DIVAC, I. Functions of the caudate nucleus. Actu biol. exp., (Vurs.) 28, 107-120, 1968. 17. ROUTTENBERG,A. The two-arousal hypothesis : Reticular formation and limbic system. Psychol. Rev. 75,51-80, 1968.
Rt%mn&-Une rkponse d’orientation Btait obtenue par stimulation Blectrique de haute fr& quence (lOO/sec) de huit points situ& dans la tCte du noyau caud6 chez six chats non anesth&i6s et se d6plaGant librement. Le comportement observe ne pouvait Ctre distingub de la rkponse d’orientation determink par une stimulation acoustique nouvelle et par stimulation &ctrique de l’amygdale, de parties du cortex, et de la formation r&iculaire m&en&phalique. Les chats s’habituaient S la stimulation du noyau caud6 comme les chats le font aux &&ements sensoriels p&iph&iques n’ayant pas valeur de signal. Les m&mes faits &aient constates lors de la stimulation de l’amygdale et du cortex, tandis qu’aucun fait d’habituation n’btait observe lors de stimulations de la formation r&iculaire m&enc&phalique.
Zusammenfassung-Bei 6 unanlsthesierten, sich frei bewegenden Katzen wurden an 8 Stellen des Caudatumkopfes hochfrequente (lOO/sec) Elektrostimulationen durchgefdhrt. Man erhielt dabei von allen Reizpunkten aus Orientierungsantworten. Das beobachtete Verhalten unterschied sich nicht von Reaktionen, die man bei iiberraschenden akustischen Reizen und bei Elektrostimulation der Amygdala, bei Teilen des Cortex und bei Reiz der mesencephalen Reticularis erhielt. Die Katzen gewijhnten sich an die Caudatumreizung genauso wie andere Tiere! die sich an nicht voraussignalisierte periphere Sinnesreize anpasten. Im wesentlichen Ahnliches wurde such bei Amygdala- und Cortexreiz festgestellt, wtihrend bei Stimulierung der mesencephalen Reticularis keine Gewahnung beobachtet werden konnte.
1969, Vol. 7, pp. 313 to 318. Pergamon Pmss. Printed in England
HABITUATION OF THE ORIENTING RESPONSE ELICITED BY STIMULATION OF THE CAUDATE NUCLEUS IN THE CAT HOLCEKURSIN, HKKAN SUNDBERGand STEVENMENAKER Institute of Physiology, University of Bergen, Norway (Received 6 January 1969) Abstract-High frequency (lOO/sec) electrical stimulation of eight points in the head of the caudate nucleus in six unanesthetized, freely moving cats yielded an orienting response from all points. The behavior observed was indistinguishable from the orienting response elicited by novel, acoustic stimulation and by electrical stimulation of the amygdala, parts of cortex, and the mesencephalic reticular formation. The cats habituated to the caudate stimulation just as cats habituate to non-signal, peripheral sensory events. The same has previously been found for stimulation of amygdala and cortex, while no habituation is observed to stimulation of the mesencephalic reticular formation.
As EARLY as 1875 DANILEWSKI[I] reported that electrical stimulation of the caudate nucleus resulted in slowing of breathing and a cessation of spontaneous movements. Later research [2, 31 also describes inhibitory functions for this nucleus. KAADA[4] described two general types of inhibitory phenomena elicited by electrical stimulation, a short lasting arrest with no loss of muscle tone, and a long lasting inhibition with loss of muscle tone. In later work, KAADAand collaborators found that the short lasting arrest observed during anesthesia is a part of the orienting response. When these “arrest” zones are stimulated in freely moving cats, the whole orienting response is seen; there is initial arrest of ongoing activity followed by orienting movements, behavioral arousal and electroencephalographic desynchronization [5-71. The present report deals with two questions: Is the behavior response elicited by electrical stimulation of the caudate nucleus of a broad inhibitory nature, or is the response identical to the orienting responses we have observed from the stimulation of other structures? If orienting responses are elicited, are they subject to habituation in the same way as those elicited by stimulation of the other arrest areas [8], or do associated inhibitory phenomena interfere with gradual disappearance of the orienting response? MATERIALS
AND METHODS
A total of 8 electrodes in 6 cats constitute the material. Electrodes were implanted during anesthesia by the ordinary stereotaxic procedure. Electrodes were 0.18 mm thin platinum wires covered by Teflon except for 1 mm at the tip, protruding into the brain tissue through a stainless steel catheter of 0.6 mm bore. This shielding served as ground for the unipolar stimulation. The animal was stimulated while freely moving in an observation chamber (45 x 55 x 145 cm) surrounded by a one-way mirror on one side, and conventional mirrors on the other three sides. The cats were stimulated by a radiocontrolled stimulator [9]. A “stimoceiver” carried by the cat weighed 14 g including battery. The stimoceivers were found ,to work reliably, producing constant current rectangular pulses. Pulse width, 313
HOLGER URSIN, H~KAN SUNDBEROand STEVENMENAKER
314
frequency and amplitude could be controlled from the radio transmitter. The frequency used was lOO/sec of 1 msec duration. The observation chamber, two observers, and the radio transmitter were placed inside an electrically shielded and sound-attenuated room. The intensity of the orienting response was evaluated by a scoring method described previously. Briefly, it consisted of four categories of behavior (see Table 1, modified from ROELOFFSet al. [lo]). The level of arousal was evaluated just before stimulus onset, and a second score was given for the behavior during and immediately after the stimulation. The difference between these two scores has been used as an indicator for the arousal effect of stimulation. Table 1. Scoring schedule
Points
Head
Eye-lids
Pars
6
Posture Running
5
Searching
Walking
4
Turning
Open
3
Lifted
Half open
2
Quiet
Membrana contracted
1
Laid down
Closed
Standing
nict.
Moving
Sitting
Quiet
Lying on belly
Curled up or lying on side
The cats had not been used for other experiments before the operation. At least 48 hours after screening the effects from the various electrode sites, avoiding unnecessary stimulation, habituation sessions were run for all electrode sites yielding clear-cut orienting responses. Stimulation intensity was chosen separately for each site as the lowest intensity giving a pre- and post-stimulatoty difference of at least 3 points in the behavior score. Intertrial intervals varied from 30 set to several minutes, a stimulus was never given unless the cat was quiet (behavior score less than 9). Habituation was said to occur when the cat, for three trials in a row, did not show more than 0.5 in the difference between the pre-and post-stimulation score. Dishabituation was then produced by introducing other arousal stimuli, and the number of trials necessary to produce rehabituation was tested for most electrodes. At the end of the experiment the animals were killed, the brains perfused and the electrode sites identified histologically in N&l-stained material.
RESULTS Caudate orienting responses
Electrical stimulation of the caudate nucleus elicited highly predictable changes in behavior. Any ongoing activity was stopped immediately at the stimulus onset, once threshold had been reached (“arrest”). Then the eyes were opened, the ears were moved forward, and the head was lifted and turned to the side opposite of that stimulated. This head movement was often slow, stepwise, and oscillating, and was referred to as “searching” in the scoring categories. The cat often sat up and moved around at higher intensities. The time course depended on the stimulation intensity. The response was adequately described by the scoring categories shown in Table 1, and is indistinguishable from the response (“orienting response”) seen when a cat is subjected to any novel stimulus. Other responses
One additional electrode, situated dorsally in the left caudate nucleus, yielded no observable orienting response. During stimulation, simple motor movements such as turning around the body axis, chewing, and mouth opening were observed. Following
WI3 OBIENTINQ BESPONSE ELICITBD BY STIMULATION OF THB CAUDATE NUCLEUS IN THE CAT
315
stimulation, the cat seemed alerted but no clearcut orienting response was observed. In addition to orienting responses at low current intensity for other sites, a stronger stimulation sometimes led to after-discharges and, occasionally, to full fledged tonic-clonic fits. Habituation to stimulation of the caudate nucleus
Repeated stimulation of the caudate nucleus invariably led to gradual disappearance of the orienting behavior (Fig. 1). A declining slope followed the waxing and waning pattern described as occurring with external stimuli and with electrical stimulation of the amygdala and the cortex [8]. A 15
I
(poinI8)
I
10 t
s I _
J
I .A
1”
I
,
I
I
13
ao
2,
._
__
Stim. no
C
Stim. m
sum. no
FIN. 1. Habituation to electrical stimulation of three points (A, B and C) in the caudate nucleus. Open circle: level of arousal before stimulation; open triangle: maximum intensity of orienting response during or immediately following the stimulation; filled circle: no orienting behavior to stimulation. Dishabituation indicated by stippled line. A drop in base line was sometimes observed (A), but this was not a necessary condition for habituation to occur (B). When very few trials were necessary to reach habituation, dishabituation sometimes was difficult to obtain without prolonging the inter-trial interval, or using very intense dishabituating stimuli (C).
The number of trials (Fig. 2) required for habituation of the caudate sites was very close to that required for the amygdala sites, and slightly lower than the level observed for cortical stimulation sites [8].
316
HOLGER URSIN,H~KANSUNDBERG
and STEVENMENAKER
FIG. 2. Frontal sections. Localization of points stimulated indicated by circles, the number inside the circle indicates number of stimulus presentations necessary to reach habituation. A and B, present material; C previously published material [8]. CA, anterior commisure; CAUD, caudate nucleus; CC, corpus callosum; CL, internal capsule; CL, claustrum; DB, diagonal band; Fx, fornix; NA, accumbens; Put, putamen; S, septum; Th, thalamus; V, ventricle.
Dishabituation
When the habituation criteria had been reached the response to stimulation of the caudate nucleus returned again when arousal was produced by some other stimulus, such as knocking on the observation cage. This phenomenon, “dishabituation”, is also illustrated in Fig. 1. When habituation then was again produced by repeating the stimulation, fewer trials were required than for the original habituation. Changing the stimulus parameters also had the same effect. The dishabituating effect did not seem to depend on the kind of stimulus used. These findings are similar to the findings for cortical and amygdala stimulation. Localization
The placement of the electrode sites is shown in Fig. 2. No differential localization of function within the caudate nucleus was observed in the present material. Intecference with ongoing eating
Stimulation of caudate sites in 3 cats during eating showed no evidence of facilitation or inhibition of food intake except for the arrest associated with the orienting response. Consequently, this incidental inhibition of eating disappeared as habituation to the caudate stimulation took place. The same type of interference, limited to arrest and responsecompetition with the orienting response, was seen in four cats where caudate stimulation was given during performance of a learned food-approach response in a Wisconsin General Test Apparatus. DISCUSSION Several authors have pointed out that the behavioral effects observed with stimulation of the caudate nucleus depend on the frequency used [2, 111. Low frequency stimulation in this area, as in many other areas of the brain, elicits a variety of “inhibitory” and sleeplike phenomena that will not be discussed here. In this paper, we are only concerned with the effects of high frequency stimulation of the caudate.
THE ORIJMTING RESPONSE ELICITED BY
STIMULATION OFTHE
CAUDATB NUCLEUS IN THE CAT
317
Contralateral head-turning and circling have been described by most reports on the effects of caudate nucleus stimulation in the freely moving cat. In fact, LAURSEN[12] claimed that these were the only “motor” responses of caudate origin. LAUR~ENfurther stated that the cats looked as if they were searching for something, and he interpreted this response as a complex behavioral manifestation rather than a stereotyped movement. It is our conclusion that this response, observed by most authors with high frequency stimulation, is the same behavior that we have called the orienting response. This has also been suggested by GALEANOet trl. [13]. This response is similar to that elicited by stimulation of the amygdala, the cortex or the mesencephalic reticular formation. In our experience, it is also indistinguishable from the orienting response observed when a novel sound is presented to a cat. It is impossible for us to tell from the observed behavior whether a given orienting response is being elicited by external stimulation or brain stimulation. In none of the electrode sites studied was there any evidence of “inhibitory” phenomena such as eye closure, lying down, or other evidence of sleep or “de-arousal”. The only “inhibitory” phenomena observed were the arrest response that is a part of the orienting response, and the habituation to the stimulation. In other words, there was no additional “inhibition” to the caudate response as compared to the orienting response elicited by external sound or electrical stimulation in the amygdala or over the lateral or supra-sylvian gyrus [81. The gradual decrease of the orienting responses to caudate stimulation is considered to be habituation since the response re-occurred when arousal was produced by some other stimulus. This phenomenon is called “dishabituation”, and is commonly regarded as a necessary condition for concluding that habituation was present [14]. It should be kept in mind that the present habituation concept is limited to decrements in the orienting response, and is not used indiscriminately for any or all response decrements [15]. The presence of dishabituation is a strong argument against interpretations of the response decrement as being due to such artifactual things as polarization of the electrode or damage to the nervous tissue by electrolytical effects. The orienting response elicited by brain stimulation and showing the habituation phenomenon, should not, in our opinion, be interpreted as a motor response elicited from “arousal areas”. The orienting response is the fixed action pattern of any cat to any novel stimulus. Any experience the brain is not “set” to expect will elicit this response. Therefore, it is to be expected that this response will be elicited by stimulation of many different types of functional systems within the brain. There is, therefore, no serious discrepancy between the demonstration of organization within the caudate nucleus discussed by DIVAC[16] and our lack of finding any localization. The experience elicited by caudate stimulation seems to be treated in the same way as adequate sensory stimulation since the response shows the habituation phenomenon. In other words, the brain may identify such stimulations as “non-signals” and stops reacting to them. By contrast, stimulation of the mesencephalic reticular formation does not habituate [8]. In this latter case, therefore, it is most likely that one is dealing with an arousal motor. Still a third way of producing arousal by stimulation of the brain is to interfere with the systems involved in motivational and emotional responses. This has been suggested as a separate arousal system by ROL’TTJZN~ERG [17], and is probably the way arousal and orienting behavior is elicited when the electrodes are close to the pericommisural parts of the septal region (Fig. 2C).
318
HOLGERURSIN,H&CAN SUNDBERG and STEVENMENAKER
REFERENCES 1. DANILEWSKY,B., JR. Experimentelle Beitrlge zur Physiologie des Gehirns. Ppiigers Arch. ges. Physiol. 11, 128-138, 1875. 2. BUCHWALD,N. A., WYERS,E. J., LAUPRECHT,C. W. and HEUSER, G. The “caudate-spindle”. IV. A behavioral index of caudate-induced inhibition. Electroenceph. ctin. Neurophysiol. 13, 531-537, 1961. 3. MET~LER,F. A., ADES, H. W., LIPMAN,E. and CULLER,E. A. The extrapyramidal system. An experimental demonstration of function. A.M.A. Archs. Neurof. Psychiut. 41,984-995, 1939. 4. KAADA, B. R. Somato-motor, autonomic and electrocorticographic responses of “rhinencephalic” and other structures in primates. cat and dog. Acta uhvsiol. scund. 24 (suo~l. 83). l-285. 1951. 5. FANGEL,C. and K~ADA, B. k. Behavior-“attentibl;” and fear induced by co&al stimulation in the cat. Electroenceph. clin. Neurophysiol. 12, 575-588, 1960. 6. KAADA, B. R. and JOHANNESSEN, N. B. Generalized electrocortical activation by cortical stimulation in the cat. Electroenceph. chin. Neurophysiol. 12, 567-573, 1960. 7. URSIN, H. and KAADA, B. R. Functional localization within the amygdaloid complex in the cat. Electroenceph. clin. Neurophysiol. 12, l-20, 1960. 8. URSIN, H., WESTER, K. and URSIN, R. Habituation to electrical stimulation of the brain in unanesthetized cats. Electroenceph. clin. Neurophysiol. 23, 4149, 1967. 9. DELGALIO, J. M. R. Aggressive behavior evoked by radio stimulation in monkey colonies. Am. ZooI. 6, 669-681, 1966. 10. ROELOFS,G. A., VANDENHOOFDAKKER,R. H. and PRECHTL,H. F. R. Sleep effects of subliminal brain stimulation in cats. Expl Neural. 8, 84-92, 1963. 11. MCLENNAN, H., EMMONS,P. R. and PLUMMER,P. M. Some behavioral effects of stimulation of the caudate nucleus in unrestrained cats. Can. J. Physiol. Pharmacol. 42, 329-339, 1964. 12. LAURSEN,A. M. Movements evoked from the region of the caudate nucleus in cats. Actu physiol. stand. 54, 175-184, 1962. J. A. Conditioning of subcortical telencephalic stimula13. GALEANO,C., ROIG, J. A. and SOMMER-SMITH, tion effects. Electroenceph. clin. Neurophysiol. 17, 281-293, 1964. 14. SOKOLOV,Y. N. Perception and the Conditioned Refi’ex. Pergamon Press, Oxford, 1963. 15. THOMPSON,R. F. and SPENCER,W. A. Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73, 16-43, 1966. 16. DIVAC, I. Functions of the caudate nucleus. Actu biol. exp., (Vurs.) 28, 107-120, 1968. 17. ROUTTENBERG,A. The two-arousal hypothesis : Reticular formation and limbic system. Psychol. Rev. 75,51-80, 1968.
Rt%mn&-Une rkponse d’orientation Btait obtenue par stimulation Blectrique de haute fr& quence (lOO/sec) de huit points situ& dans la tCte du noyau caud6 chez six chats non anesth&i6s et se d6plaGant librement. Le comportement observe ne pouvait Ctre distingub de la rkponse d’orientation determink par une stimulation acoustique nouvelle et par stimulation &ctrique de l’amygdale, de parties du cortex, et de la formation r&iculaire m&en&phalique. Les chats s’habituaient S la stimulation du noyau caud6 comme les chats le font aux &&ements sensoriels p&iph&iques n’ayant pas valeur de signal. Les m&mes faits &aient constates lors de la stimulation de l’amygdale et du cortex, tandis qu’aucun fait d’habituation n’btait observe lors de stimulations de la formation r&iculaire m&enc&phalique.
Zusammenfassung-Bei 6 unanlsthesierten, sich frei bewegenden Katzen wurden an 8 Stellen des Caudatumkopfes hochfrequente (lOO/sec) Elektrostimulationen durchgefdhrt. Man erhielt dabei von allen Reizpunkten aus Orientierungsantworten. Das beobachtete Verhalten unterschied sich nicht von Reaktionen, die man bei iiberraschenden akustischen Reizen und bei Elektrostimulation der Amygdala, bei Teilen des Cortex und bei Reiz der mesencephalen Reticularis erhielt. Die Katzen gewijhnten sich an die Caudatumreizung genauso wie andere Tiere! die sich an nicht voraussignalisierte periphere Sinnesreize anpasten. Im wesentlichen Ahnliches wurde such bei Amygdala- und Cortexreiz festgestellt, wtihrend bei Stimulierung der mesencephalen Reticularis keine Gewahnung beobachtet werden konnte.