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Aftereffects of rewarding lateral hypothalamic brain stimulation and feeding behavior
Physiology & Behavior, Vol. 17, pp. 865--867. Pergamon Press and Brain Research Publ., 1976. Printed in the U.S.A.
BRIEF COMMUNICATION Aftereffects of Rewarding Lateral Hypothalamic Brain Stimulation and Feeding Behavior 1 JAMES R. S T E L L A R 2 AND KAREN H E A R D
University o f Pennsylvania, Philadelphia, PA 191 74 (Received 15 January 1976) STELLAR, J. R. AND K. HEARD. Aftereffects of rewarding lateral hypothalamic brain stimulation and feeding behavior. PHYSIOL. BEHAV. 17(5) 865-867, 1976. - The aftereffects of rewarding lateral hypothalamic brain stimulation are shown to depress the speed with which rats will initiate consumption of various foods. The strength of this depression was positively correlated (rxy = 0.60) with the rate of self-stimulation on that electrode. Seemingly paradoxical relations between this finding andother known characteristics of lateral hypothalamic stimulation are discussed. Lateral hypothalamic stimulation
Self-stimulation
Aftereffects
MANIPULATIONS that increase the hunger of an animal also increase its self-stimulation performance for lateral hypothalamic (LH) brain stimulation [3]. An earlier report [5] demonstrated that hunger elevated self-stimulation performance by summing with or enhancing the priming effect rather than the rewarding effect of LH stimulation. A somewhat paradoxical finding in the same report was that the priming effect of LH stimulation suppressed performance for a food reward. Thus, priming and hunger both enhance performance for brain stimulation reward, but they act oppositely on performance for food reward. We examined this priming-induced suppression of foodseeking behavior in an environment where feeding behavior was made very likely by (1) exposing hungry rats, at close quarters, to large amounts of their normal food, lab chow, and (2) exposing hungry rats to foods of high palatability. We also tested for any relationship between the magnitude of the depression of feeding produced by priming on a given electrode and the strength of self-stimulation behavior on that electrode.
Feeding depression
Under Equi-Thesian anesthetic (0.03 cc/kg), each rat was implanted with an assembly of 5 monopolar electrodes aimed at various sites along the medial forebrain bundle. A skull surface ground wire was included. At the conclusion of the experiment, brain histology was performed and location of electrode tips were plotted on the Konig and Klippel [4] atlas of the rat brain (Fig. 1).
Procedure The experiment was divided into three phases: Phase I tested for stimulus-elicited behaviors; Phase II tested for self-stimulation; and Phase III tested for feeding behavior after receipt of brain stimulation. Throughout the experiment, unless otherwise specified, a burst of brain stimulation consisted of monophasic rectangular pulses 0.1 msec wide, maintained at 2.5 V by a constant voltage stimulator, and delivered at a rate of 100 pulses per sec. A 502-A Tektronix oscilloscope was used to monitor the voltage of the stimulating electrode and to calculate the current flow through the electrode by monitoring the vol-tage drop across a 100 s2 resistor placed in series with the rat. In Phase I each rat was tested on each electrode for stimulation-elicited eating, drinking, and gnawing. Testing was conducted by administering 30 sec of brain stimulation in the home cage with food, water, and wooden blocks continuously available. A variety of stimulation current
METHOD
Animals The animals were 5 male albino rats from Charles River Laboratories, weighing between 3 0 0 - 5 0 0 g and maintained in a 24-hr light-dark reversed cycle. All testing was conducted in dim red light during the animal's dark period.
~This work was supported by NIGMS Grant No. 5T01-GM-01036-14. The authors wish to thank Michael Matthews, C. R. GaUistel, Joseph Liran and Linda E. Mills for reading and criticizing earlier drafts of this paper. 2All reprint requests should be directed to the Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19174. 865
866
KHB2N'*
STELLAR AND HEARD
f
JSd'l 7"[f'
FIG. 1. Histological location of electrode tips are plotted on drawings from Konig and Klippel atlas of the rat brain. Numbers in the upper right of each drawing indicate the Konig and Klippel plate number. levels were used (range = 100 -+ 50 u A ) and each c u r r e n t level was given several tests. All electrodes sustaining a n y stimulus-elicited eating, drinking, or g n a w i n g were i n c l u d e d in t h e study. In Phase II e a c h a n i m a l was t r a i n e d to press a lever for 1/3 sec b u r s t of brain s t i m u l a t i o n o n o n e o f its electrodes. Training was c o n c l u d e d w h e n the lever-pressing rates r e a c h e d a stable a s y m p t o t e . S e l f - s t i m u l a t i o n rate was m e a s u r e d b y e x p o s i n g t h e rat t o t h e lever a n d c o u n t i n g t h e t o t a l n u m b e r of r e w a r d e d lever presses t h a t o c c u r r e d in a 5 m i n period. T h e m e a n n u m b e r of presses per m i n u t e was t h e n d e t e r m i n e d for this electrode. This p r o c e d u r e was r e p e a t e d for all electrodes in e a c h rat. T h r e e electrodes in each rat were selected b y t h e e x p e r i m e n t e r s for use in Phase III so as to o b t a i n a wide range of s e l f - s t i m u l a t i o n rates b o t h w i t h i n a n d across animals. In Phase Ill of t h e e x p e r i m e n t , t h e a f t e r e f f e c t s o f r e w a r d i n g b r a i n s t i m u l a t i o n o n feeding b e h a v i o r were tested. During this phase, rats were always t r a i n e d a n d tested while 2 0 - 2 3 hr f o o d deprived. In t r a i n i n g trials, each rat was placed in o n e c o m e r of its o w n p l y w o o d b o x facing t h e o p p o s i t e diagonal corner, which c o n t a i n e d a pile of a b o u t 30 lab c h o w pellets. L a t e n c y to eat was m e a s u r e d w i t h a s t o p w a t c h f r o m t h e t i m e t h e r a t ' s feet h i t t h e floor u n t i l its first bite of food. The rat was t h e n given 15 sec to eat b e f o r e b e i n g r e m o v e d from t h e box. If t h e l a t e n c y e x c e e d e d 60 sec, t h e a n i m a l
was placed o n the f o o d pile. Five m i n elapsed before a n o t h e r trial was run. All latencies were t r a n s f o r m e d i n t o their inverses to yield speed scores a n d will be referred to as such t h r o u g h o u t t h e r e m a i n d e r of this r e p o r t . T r a i n i n g was c o n t i n u e d u n t i l t h e speeds h a d r e a c h e d a n a s y m p t o t e . During t e s t i n g in this p h a s e of the e x p e r i m e n t , rats were first given a p r e p r o g r a m m e d t r a i n of p r i m i n g b r a i n stimN a t i o n . T h e y were t h e n placed in t h e i r p l y w o o d b o x a n d r u n a c c o r d i n g to the same p r o c e d u r e described for t h e training. T h e p r i m i n g t r a i n consisted o f t e n b u r s t s of 64 pulses w i t h the b u r s t s being delivered at the rate o f I per sec. All o t h e r p a r a m e t e r s of t h e s t i m u l a t i o n were as previously stated. This t y p e of p r i m i n g h a s b e e n f o u n d to be effective in p r o d u c i n g a s t r o n g m o t i v a t i o n - l i k e aftereffect w h e n rats are r u n n i n g a n alley for b r a i n s t i m u l a t i o n reward [ 21. E a c h rat was r u n 4 trials per day w i t h at least a 10 m i n intertrial interval. T h r e e of t h e trials assessed the effect o f p r i m i n g f r o m o n e of t h e t h r e e electrodes, o n e e l e c t r o d e being t e s t e d per trial. T h e o t h e r trial was a n o - p r i m i n g trial. Thus, for each rat, all t h r e e electrodes were t e s t e d each day and t h e u n p r i m e d baseline was m e a s u r e d daily. All trials w i t h i n a day were r u n in a s y s t e m a t i c a l l y varying p a t t e r n designed to e l i m i n a t e o r d e r effects. This p r o c e d u r e was c o n t i n u e d for 10 days w i t h lab c h o w serving as t h e food. The rats were t h e n s w i t c h e d t o t h e following highly palatable foods: JS No. 18 a n d KH No. 1 received c a n n e d dog f o o d ( m e a t ) ; JS No. 17 and KH No. 2 received sweet c h o c o l a t e ; a n d JS No. 19 received c h o c o l a t e chip cookies soaked in milk. T h e y were r e t r a i n e d to t h e new f o o d s in exactly t h e same m a n n e r as t h e y were t r a i n e d to the lab c h o w in t h e b e g i n n i n g of Phase III of t h e e x p e r i m e n t . A f t e r the speeds h a d again stabilized, t h e rats were tested in t h e same m a n n e r as w i t h t h e lab chow. A t t h e c o n c l u s i o n of t h e testing w i t h p a l a t a b l e foods, all rats were r e t r a i n e d to lab c h o w a n d r u n as before e x c e p t t h a t o n l y 5 days of data were collected. This was d o n e to c h e c k the possibility t h a t a n y increased speed in t h e palatable f o o d c o n d i t i o n was due to a general learning effect n o t o v e r c o m e b y t h e original training sessions. RESULTS In Phase I of t h e e x p e r i m e n t several b r a i n stimulation-elicited b e h a v i o r s were f o u n d . JS No. 17 e x h i b i t e d d r i n k i n g o n e l e c t r o d e E a n d KH No. 2 e x h i b i t e d g n a w i n g on electrode C. T h e results of Phase III a n d t h e i r statistical analysis are p r e s e n t e d in Fig. 2. On a m a j o r i t y of t h e electrodes tested, pretrial ( p r i m i n g ) b r a i n s t i m u l a t i o n caused a significant r e d u c t i o n in t h e speed w i t h w h i c h rats i n i t i a t e d t h e c o n s u m p t i o n of lab c h o w and m o r e p a l a t a b l e foods. Priming s t i m u l a t i o n n e v e r caused a significant increase in speed. All statistical c o m p a r i s o n s were m a d e b e t w e e n t h e u n p r i m e d and p r i m e d c o n d i t i o n s w i t h i n o n e a n i m a l a n d w i t h i n o n e t y p e of f o o d c o n d i t i o n . A n e x a c t p r o b a b i l i t y M a n n - W h i t n e y U test was e m p l o y e d ; the resulting p values are r e p o r t e d in Fig. 2. A l t h o u g h m e a n speed in the n o p r i m i n g c o n d i t i o n increased w h e n t h e animals were s w i t c h e d f r o m lab c h o w to palatable foods, in o n l y o n e animal, KH No. 2, did this increase r e a c h statistical significance ( p < 0 . 0 0 1 , M a n n W h i t n e y U test). W h e n t h e animals were r e t u r n e d to lab c h o w , all a n i m a l s e x c e p t KH No. 1 s h o w e d a significant decrease in speed ( p < 0 . 0 1 , M a n n - W h i t n e y U test). T h u s t h e
REWARDING STIMULATION A F T E R E F F E C T S AND F EED I N G
Palatable Foods Lab Chow
Lab Chow (Fast)
(Slow)
0.2
I JS017
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0
NP
C
i
D
NP
F
C
0.4 JS#18
i
O
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!--!--'--R:,, o0o
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.022
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,I
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NP
~
.0005 2
)
E
F
J
H
NP
_ -
H
867
was performed. Priming-induced reductions in speed were expressed as z-scores to equate for differences in within animal variability, so that scores could be compared across animals. Z-score transformation was accomplished by Xnp.~Xp, applying the following formula: z where Xnp = mean speed in the no priming condition, Xp = mean speed after priming on a given electrode, and o = average within session standard deviation for that animal. The correlation coefficient was positive and statistically significant (rxy = 0.60, p<0.02 s). Because the brain stimulation was of the constant voltage type and the electrode resistance varied slightly, stimulating current varied slightly across electrodes. However, a correlation coefficient computed between stimulating current levels and lever-pressing rates was found to be non-significant (rxy = - 0 . 0 1 , p>0.10). A correlation computed between stimulating current and the magnitude of the priming-induced depression of feeding was also not significant (rxy = - 0 . 0 1 , p> 0.10). This does not mean that stimulating current has no effect on either of these variables but rather that over the small ranges considered here stimulating current is not an important consideration. DISCUSSION
I-I
NP
E
F
H
NP
E
F
H
NP
[-I .... -------
F KH#2
.026
0.2
........
I
.053 .072 - 0
NP
A
C
H
I
I
NP
A
C
H
NP
FIG. 2. Mean speed to initiate consumption of food with and without pretrial (priming) stimulation is plotted as the height of the bars. The NP bars indicate speed on the trials without priming. The letters under the bars indicate the electrode through which priming stimulation was delivered. The significance of the difference between performance when primed on a given electrode and performance in the absence of priming was assessed with an exact probability Mann-Whitney U test. The p values appear above the appropriate solid bars. increase in speed to palatable foods did not appear to be due to growing familiarity with the testing situation. To test for a relationship between the priming-induced reduction in speed to initiate consumption of lab chow and the rate of self-stimulation on that electrode, a correlation
These results show that pretrial rewarding lateral hypothalamic brain stimulation decreases the speed with which a hungry rat will initiate consumption of abundant, nearby foods of various palatabilities. This result is in agreement with other reports [ 1,5]. Also, the vigor with which a rat will self-stimulate on a given electrode is positively and significantly correlated with the depression of feeding induced by pretrial priming stimulation on a given electrode. This finding argues for some relationship between the neural substrates underlying the two effects. The apparent relation between self-stimulation and the depression of feeding by priming stimulation poses the following paradox: stimulation of the lateral hypothalamus frequently increases a rat's tendency to approach and consume food (stimulation-elicited feeding). This stimulation is usually rewarding (self-stimulation) and leaves behind a decaying aftereffect that promotes approach to and consumption of brain-stimulation reward (the priming effect). Thus, the effect of priming on self-stimulation behavior resembles the effect of hunger on food-rewarded behavior. Furthermore, hunger summates with the priming effect when the reward is brain stimulation. However, when the reward is food, hunger and priming act in opposite directions. Hunger promotes the approach to and consumption of food, whereas priming inhibits both.
REFERENCES 1. 2.
3.
Cox, V. C., J. W. Kakolewski and E. S. Valenstein. Inhibition of eating and drinking following hypothalamic stimulation in the rat. J. camp. physiol. Psychol. 68: 530-535, 1969. Galiistel, C. R. Self-stimulation: The neurophysiology of reward and motivation. In: The Physiological Basis of Memory, edited by J. A. Deutsch, New York: Academic Press, 1973, pp. 175-267. Hoebel, B. G. Inhibition and disinhibition of self-stimulation and feeding: Hypothalamic control and postingestional factors. J. camp. physiol. Psychol. 66: 89-100, 1968.
4. 5.
Konig, J. F. R., and R. A. Klippel. The Rat Brain: A Stereotaxic Atlas Baltimore: Williams and Williams, 1963. Stellar, J. R. and C. R. Gallistel. Runway performance of rats for brain stimulation or food reward: Effects of hunger and priming. J. camp. physiol. Psychol. 89: 590-599, 1975.
BRIEF COMMUNICATION Aftereffects of Rewarding Lateral Hypothalamic Brain Stimulation and Feeding Behavior 1 JAMES R. S T E L L A R 2 AND KAREN H E A R D
University o f Pennsylvania, Philadelphia, PA 191 74 (Received 15 January 1976) STELLAR, J. R. AND K. HEARD. Aftereffects of rewarding lateral hypothalamic brain stimulation and feeding behavior. PHYSIOL. BEHAV. 17(5) 865-867, 1976. - The aftereffects of rewarding lateral hypothalamic brain stimulation are shown to depress the speed with which rats will initiate consumption of various foods. The strength of this depression was positively correlated (rxy = 0.60) with the rate of self-stimulation on that electrode. Seemingly paradoxical relations between this finding andother known characteristics of lateral hypothalamic stimulation are discussed. Lateral hypothalamic stimulation
Self-stimulation
Aftereffects
MANIPULATIONS that increase the hunger of an animal also increase its self-stimulation performance for lateral hypothalamic (LH) brain stimulation [3]. An earlier report [5] demonstrated that hunger elevated self-stimulation performance by summing with or enhancing the priming effect rather than the rewarding effect of LH stimulation. A somewhat paradoxical finding in the same report was that the priming effect of LH stimulation suppressed performance for a food reward. Thus, priming and hunger both enhance performance for brain stimulation reward, but they act oppositely on performance for food reward. We examined this priming-induced suppression of foodseeking behavior in an environment where feeding behavior was made very likely by (1) exposing hungry rats, at close quarters, to large amounts of their normal food, lab chow, and (2) exposing hungry rats to foods of high palatability. We also tested for any relationship between the magnitude of the depression of feeding produced by priming on a given electrode and the strength of self-stimulation behavior on that electrode.
Feeding depression
Under Equi-Thesian anesthetic (0.03 cc/kg), each rat was implanted with an assembly of 5 monopolar electrodes aimed at various sites along the medial forebrain bundle. A skull surface ground wire was included. At the conclusion of the experiment, brain histology was performed and location of electrode tips were plotted on the Konig and Klippel [4] atlas of the rat brain (Fig. 1).
Procedure The experiment was divided into three phases: Phase I tested for stimulus-elicited behaviors; Phase II tested for self-stimulation; and Phase III tested for feeding behavior after receipt of brain stimulation. Throughout the experiment, unless otherwise specified, a burst of brain stimulation consisted of monophasic rectangular pulses 0.1 msec wide, maintained at 2.5 V by a constant voltage stimulator, and delivered at a rate of 100 pulses per sec. A 502-A Tektronix oscilloscope was used to monitor the voltage of the stimulating electrode and to calculate the current flow through the electrode by monitoring the vol-tage drop across a 100 s2 resistor placed in series with the rat. In Phase I each rat was tested on each electrode for stimulation-elicited eating, drinking, and gnawing. Testing was conducted by administering 30 sec of brain stimulation in the home cage with food, water, and wooden blocks continuously available. A variety of stimulation current
METHOD
Animals The animals were 5 male albino rats from Charles River Laboratories, weighing between 3 0 0 - 5 0 0 g and maintained in a 24-hr light-dark reversed cycle. All testing was conducted in dim red light during the animal's dark period.
~This work was supported by NIGMS Grant No. 5T01-GM-01036-14. The authors wish to thank Michael Matthews, C. R. GaUistel, Joseph Liran and Linda E. Mills for reading and criticizing earlier drafts of this paper. 2All reprint requests should be directed to the Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19174. 865
866
KHB2N'*
STELLAR AND HEARD
f
JSd'l 7"[f'
FIG. 1. Histological location of electrode tips are plotted on drawings from Konig and Klippel atlas of the rat brain. Numbers in the upper right of each drawing indicate the Konig and Klippel plate number. levels were used (range = 100 -+ 50 u A ) and each c u r r e n t level was given several tests. All electrodes sustaining a n y stimulus-elicited eating, drinking, or g n a w i n g were i n c l u d e d in t h e study. In Phase II e a c h a n i m a l was t r a i n e d to press a lever for 1/3 sec b u r s t of brain s t i m u l a t i o n o n o n e o f its electrodes. Training was c o n c l u d e d w h e n the lever-pressing rates r e a c h e d a stable a s y m p t o t e . S e l f - s t i m u l a t i o n rate was m e a s u r e d b y e x p o s i n g t h e rat t o t h e lever a n d c o u n t i n g t h e t o t a l n u m b e r of r e w a r d e d lever presses t h a t o c c u r r e d in a 5 m i n period. T h e m e a n n u m b e r of presses per m i n u t e was t h e n d e t e r m i n e d for this electrode. This p r o c e d u r e was r e p e a t e d for all electrodes in e a c h rat. T h r e e electrodes in each rat were selected b y t h e e x p e r i m e n t e r s for use in Phase III so as to o b t a i n a wide range of s e l f - s t i m u l a t i o n rates b o t h w i t h i n a n d across animals. In Phase Ill of t h e e x p e r i m e n t , t h e a f t e r e f f e c t s o f r e w a r d i n g b r a i n s t i m u l a t i o n o n feeding b e h a v i o r were tested. During this phase, rats were always t r a i n e d a n d tested while 2 0 - 2 3 hr f o o d deprived. In t r a i n i n g trials, each rat was placed in o n e c o m e r of its o w n p l y w o o d b o x facing t h e o p p o s i t e diagonal corner, which c o n t a i n e d a pile of a b o u t 30 lab c h o w pellets. L a t e n c y to eat was m e a s u r e d w i t h a s t o p w a t c h f r o m t h e t i m e t h e r a t ' s feet h i t t h e floor u n t i l its first bite of food. The rat was t h e n given 15 sec to eat b e f o r e b e i n g r e m o v e d from t h e box. If t h e l a t e n c y e x c e e d e d 60 sec, t h e a n i m a l
was placed o n the f o o d pile. Five m i n elapsed before a n o t h e r trial was run. All latencies were t r a n s f o r m e d i n t o their inverses to yield speed scores a n d will be referred to as such t h r o u g h o u t t h e r e m a i n d e r of this r e p o r t . T r a i n i n g was c o n t i n u e d u n t i l t h e speeds h a d r e a c h e d a n a s y m p t o t e . During t e s t i n g in this p h a s e of the e x p e r i m e n t , rats were first given a p r e p r o g r a m m e d t r a i n of p r i m i n g b r a i n stimN a t i o n . T h e y were t h e n placed in t h e i r p l y w o o d b o x a n d r u n a c c o r d i n g to the same p r o c e d u r e described for t h e training. T h e p r i m i n g t r a i n consisted o f t e n b u r s t s of 64 pulses w i t h the b u r s t s being delivered at the rate o f I per sec. All o t h e r p a r a m e t e r s of t h e s t i m u l a t i o n were as previously stated. This t y p e of p r i m i n g h a s b e e n f o u n d to be effective in p r o d u c i n g a s t r o n g m o t i v a t i o n - l i k e aftereffect w h e n rats are r u n n i n g a n alley for b r a i n s t i m u l a t i o n reward [ 21. E a c h rat was r u n 4 trials per day w i t h at least a 10 m i n intertrial interval. T h r e e of t h e trials assessed the effect o f p r i m i n g f r o m o n e of t h e t h r e e electrodes, o n e e l e c t r o d e being t e s t e d per trial. T h e o t h e r trial was a n o - p r i m i n g trial. Thus, for each rat, all t h r e e electrodes were t e s t e d each day and t h e u n p r i m e d baseline was m e a s u r e d daily. All trials w i t h i n a day were r u n in a s y s t e m a t i c a l l y varying p a t t e r n designed to e l i m i n a t e o r d e r effects. This p r o c e d u r e was c o n t i n u e d for 10 days w i t h lab c h o w serving as t h e food. The rats were t h e n s w i t c h e d t o t h e following highly palatable foods: JS No. 18 a n d KH No. 1 received c a n n e d dog f o o d ( m e a t ) ; JS No. 17 and KH No. 2 received sweet c h o c o l a t e ; a n d JS No. 19 received c h o c o l a t e chip cookies soaked in milk. T h e y were r e t r a i n e d to t h e new f o o d s in exactly t h e same m a n n e r as t h e y were t r a i n e d to the lab c h o w in t h e b e g i n n i n g of Phase III of t h e e x p e r i m e n t . A f t e r the speeds h a d again stabilized, t h e rats were tested in t h e same m a n n e r as w i t h t h e lab chow. A t t h e c o n c l u s i o n of t h e testing w i t h p a l a t a b l e foods, all rats were r e t r a i n e d to lab c h o w a n d r u n as before e x c e p t t h a t o n l y 5 days of data were collected. This was d o n e to c h e c k the possibility t h a t a n y increased speed in t h e palatable f o o d c o n d i t i o n was due to a general learning effect n o t o v e r c o m e b y t h e original training sessions. RESULTS In Phase I of t h e e x p e r i m e n t several b r a i n stimulation-elicited b e h a v i o r s were f o u n d . JS No. 17 e x h i b i t e d d r i n k i n g o n e l e c t r o d e E a n d KH No. 2 e x h i b i t e d g n a w i n g on electrode C. T h e results of Phase III a n d t h e i r statistical analysis are p r e s e n t e d in Fig. 2. On a m a j o r i t y of t h e electrodes tested, pretrial ( p r i m i n g ) b r a i n s t i m u l a t i o n caused a significant r e d u c t i o n in t h e speed w i t h w h i c h rats i n i t i a t e d t h e c o n s u m p t i o n of lab c h o w and m o r e p a l a t a b l e foods. Priming s t i m u l a t i o n n e v e r caused a significant increase in speed. All statistical c o m p a r i s o n s were m a d e b e t w e e n t h e u n p r i m e d and p r i m e d c o n d i t i o n s w i t h i n o n e a n i m a l a n d w i t h i n o n e t y p e of f o o d c o n d i t i o n . A n e x a c t p r o b a b i l i t y M a n n - W h i t n e y U test was e m p l o y e d ; the resulting p values are r e p o r t e d in Fig. 2. A l t h o u g h m e a n speed in the n o p r i m i n g c o n d i t i o n increased w h e n t h e animals were s w i t c h e d f r o m lab c h o w to palatable foods, in o n l y o n e animal, KH No. 2, did this increase r e a c h statistical significance ( p < 0 . 0 0 1 , M a n n W h i t n e y U test). W h e n t h e animals were r e t u r n e d to lab c h o w , all a n i m a l s e x c e p t KH No. 1 s h o w e d a significant decrease in speed ( p < 0 . 0 1 , M a n n - W h i t n e y U test). T h u s t h e
REWARDING STIMULATION A F T E R E F F E C T S AND F EED I N G
Palatable Foods Lab Chow
Lab Chow (Fast)
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was performed. Priming-induced reductions in speed were expressed as z-scores to equate for differences in within animal variability, so that scores could be compared across animals. Z-score transformation was accomplished by Xnp.~Xp, applying the following formula: z where Xnp = mean speed in the no priming condition, Xp = mean speed after priming on a given electrode, and o = average within session standard deviation for that animal. The correlation coefficient was positive and statistically significant (rxy = 0.60, p<0.02 s). Because the brain stimulation was of the constant voltage type and the electrode resistance varied slightly, stimulating current varied slightly across electrodes. However, a correlation coefficient computed between stimulating current levels and lever-pressing rates was found to be non-significant (rxy = - 0 . 0 1 , p>0.10). A correlation computed between stimulating current and the magnitude of the priming-induced depression of feeding was also not significant (rxy = - 0 . 0 1 , p> 0.10). This does not mean that stimulating current has no effect on either of these variables but rather that over the small ranges considered here stimulating current is not an important consideration. DISCUSSION
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FIG. 2. Mean speed to initiate consumption of food with and without pretrial (priming) stimulation is plotted as the height of the bars. The NP bars indicate speed on the trials without priming. The letters under the bars indicate the electrode through which priming stimulation was delivered. The significance of the difference between performance when primed on a given electrode and performance in the absence of priming was assessed with an exact probability Mann-Whitney U test. The p values appear above the appropriate solid bars. increase in speed to palatable foods did not appear to be due to growing familiarity with the testing situation. To test for a relationship between the priming-induced reduction in speed to initiate consumption of lab chow and the rate of self-stimulation on that electrode, a correlation
These results show that pretrial rewarding lateral hypothalamic brain stimulation decreases the speed with which a hungry rat will initiate consumption of abundant, nearby foods of various palatabilities. This result is in agreement with other reports [ 1,5]. Also, the vigor with which a rat will self-stimulate on a given electrode is positively and significantly correlated with the depression of feeding induced by pretrial priming stimulation on a given electrode. This finding argues for some relationship between the neural substrates underlying the two effects. The apparent relation between self-stimulation and the depression of feeding by priming stimulation poses the following paradox: stimulation of the lateral hypothalamus frequently increases a rat's tendency to approach and consume food (stimulation-elicited feeding). This stimulation is usually rewarding (self-stimulation) and leaves behind a decaying aftereffect that promotes approach to and consumption of brain-stimulation reward (the priming effect). Thus, the effect of priming on self-stimulation behavior resembles the effect of hunger on food-rewarded behavior. Furthermore, hunger summates with the priming effect when the reward is brain stimulation. However, when the reward is food, hunger and priming act in opposite directions. Hunger promotes the approach to and consumption of food, whereas priming inhibits both.
REFERENCES 1. 2.
3.
Cox, V. C., J. W. Kakolewski and E. S. Valenstein. Inhibition of eating and drinking following hypothalamic stimulation in the rat. J. camp. physiol. Psychol. 68: 530-535, 1969. Galiistel, C. R. Self-stimulation: The neurophysiology of reward and motivation. In: The Physiological Basis of Memory, edited by J. A. Deutsch, New York: Academic Press, 1973, pp. 175-267. Hoebel, B. G. Inhibition and disinhibition of self-stimulation and feeding: Hypothalamic control and postingestional factors. J. camp. physiol. Psychol. 66: 89-100, 1968.
4. 5.
Konig, J. F. R., and R. A. Klippel. The Rat Brain: A Stereotaxic Atlas Baltimore: Williams and Williams, 1963. Stellar, J. R. and C. R. Gallistel. Runway performance of rats for brain stimulation or food reward: Effects of hunger and priming. J. camp. physiol. Psychol. 89: 590-599, 1975.