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The influence of control over appetitive and aversive events on alcohol preference in rats
Alcohol, Vol. 7, pp. 133--136.©PergamonPress plc, 1990. Printedin the U.S.A.
0741-8329/90$3.00 + .00
The Influence Of Control Over Appetitive and Aversive Events on Alcohol Preference in Rats J O S E P H R. V O L P I C E L L I 1
Departments of Psychiatry and Psychology, University of Pennsylvania, Philadelphia, PA 19104 AND R O N A L D R. U L M
Department of Psychology, Salisbury State University, Salisbury, MD 21801 Received 5 July 1988; Accepted 29 July 1989
VOLPICEIJ.I, J. R. AND R. R. ULM. The influence of control over appetitive and aversive events on alcoholpreference in rats. ALCOHOL 7(2) 133-136, 1990.-- The effect of control of food reinforcement or shock termination on alcohol drinking was examined in two experiments. In the In'st experiment, rats unable to control the delivery of food pellets preferred alcohol more than rats which had control over food. Similarly, in the second experiment, rats unable to control electric footshoek termination preferred alcohol more than rats which could escape shock. These results showed that the psychological dimension of control over environmental events influences alcohol preference in rats. Stress
Alcohol self-selection
Rats
Uncontrollable shock
ANIMALS and humans lacking control over aversive events exhibit a variety of behavioral and physiological changes which have been commonly referred to as helplessness effects (9). These experiments always use the yoked control procedure. This procedure involves matching pairs of subjects such that all physical stimuli are held constant, but one subject controls the presentation or termination of the important stimulus event. For example, in the typical helplessness experiment, shock presentations are identical for each pair of rats, but one of the rats can escape from shock (master rat) while shock termination occurs at the same time regardless of the behavior of its yoked partner (helpless rat). In this way, only the controllability of the important stimulus event is varied while the physical properties of the event are held constant. Thus, the duration, intensity, and pattern of shocks is identical within each pair. Using this yoked control procedure, Maier and Seligman (9) have demonstrated that uncontrollably shocked rats are more passive in new situations than rats exposed to equivalent amounts of controllable shock. Others have shown that uncontrollable shock leads to immunosuppression (7), gastric ulceration (19), decreased resistance to a tumor challenge (15), higher catecholamine and corticosterone levels (14), and higher 13-endorphin levels
Uncontrollable food
Tension reduction hypothesis
in peripheral blood (12). In the few studies which have systematically examined the influence of controllability on appetitive events, similar behavioral helplessness effects have been observed. Goodkin et al. (6) found that, following uncontrollable food pellets, rats were slower to learn a new response to obtain food reward and were more passive in a novel shock escape task than rats exposed to equivalent amounts of controllable food. Similarly, Engberg et al. (4) found that, following uncontrollable food pellets, rats were also slower to escape in a new shock escape task. There is some indication that the psychological dimension of control over environmental events may be related to alcohol drinking. Human alcoholics, for example, report feelings of lack of control over alcohol drinking as well as other aspects of their lives (2). However, there is little systematic research that investigates this relationship. One exception is a study that showed increased alcohol drinking following unsolvable problems in female social drinkers (11). Alcohol per se may lead to increased feelings of lack of control, or conversely, uncontrollable events may lead to alcoholism. The present experiments attempt to clarify this issue by systematically assessing the effects of controllability on alcohol drinking in rats.
~Requests for reprints should be addressed to Joseph R. Volpicelli, M.D., Ph.D., Addiction Research Center, 3910 Chestnut St., University of Pennsylvania, Philadelphia, PA 19104.
133
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EXPERIMENT 1: APPETITIVE CONTROL There have been several attempts to elicit excessive alcohol drinking in rats using appetitive events. For example, Falk and Samson (5), found that food-deprived rats with access to a 5% alcohol solution drank large amounts of alcohol when a food pellet was delivered uncontrollably about once every two minutes. This procedure has been termed scheduled-induced polydipsia and it has been used to induce animals to drink an excessive amount of many fluids including water. Since the controllability dimension was not systematically varied, however, it is not clear from this research whether rats drank alcohol, 1) for some reinforcing pharmacological effect of alcohol related to the lack of control over food pellets, 2) because drinking is nonspecifically directed at alcohol because it is the only fluid available or 3) to compensate for their restricted caloric schedule. Therefore, our first experiment systematically investigated the effects of controllability over food pellets using the yoked control procedure. Since alcohol preference is examined in a two-bottle test with both alcohol and water continuously available, and rats receive equivalent amounts of food, differences between the yoked and control subjects can be attributed to the psychological effects of lack of control over food. METHOD
Subjects Subjects were 10 male Sprague-Dawley rats (N=5/group) obtained from Holtzman Co., Madison, WI. Rats were obtained at 60 days of age and were individually housed and raised in a 14 hr light-10 hr dark environment. During the first seven days subjects were gradually reduced to 80% body weight and then paired according to weight and placed in operant chambers, with control versus yoked assignment randomly determined.
Apparatus Subjects lived in a modified Skinner box with a lever mounted on the front of the chamber and two graduated cylinders mounted at the rear of the chamber so that both alcohol and water were freely available at all times. Rats obtained fluid by licking narrow metal drinking spouts that protruded 2 cm into the cage. This technique was used to eliminate the spillage that can occur with other types of drinking tubes.
Procedure Following assignment into the yoked or control groups, rats were placed in operant chambers for the next 28 days. Water and 10% alcohol sweetened with 0.25% sodium saccharin was freely available to all subjects. Food pellets (45 mg Noyes pellets) were delivered to both the control and its yoked partner when the control rat pressed the lever. On day 1, each lever-press resulted in a food pellet and on subsequent days lever-pressing was reinforced on a VI-60 second schedule (range 10 to 120 sec). Since subjects in both groups ate the pellets immediately when it was delivered, the only difference between the two groups was that the control group could control food presentations by lever-pressing while the yoked rats had no control over food presentations. This appetitive schedule control feeding was in effect 24 hr/day. Dally measurements of the weight and fluid consumption of each rat were made and followed by placing a fresh supply of water or alcohol into the graduated cylinders. To avoid position biases the fluid cylinders were rotated daily. RESULTS AND DISCUSSION
In order to control for difference in total fluid consumption, the
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FIG. 1. Mean ethanol preference for rats with control over food pellets and rats which received yoked pellet presentations across 14 blocks of two-day averages.
TABLE
1
MEANS, STANDARD ERRORS, AND t-TESTS FOR WATER, ETHANOL, AND TERMINAL WEIGHT FOR THE CONTROL AND YOKED CONDITIONS OF EXPERIMENT 1
Water (ml) Ethanol (g/kg) Terminal Weight (g)
Control Group
Yoked Group
t-test
19.34 (2.19) 5.08 (0.89) 409 (10.00)
13.5 (2.09) 9.14 (0.69) 429 (8.17)
n.s. 3.21, p<0.03 n.s.
percent alcohol preference was calculated by dividing the volume of alcohol consumed by the total fluid consumed and multiplying the result by 100. Figure 1 shows the average percent alcohol preference over 14 blocks of two-day averages for the control and yoked groups. Clearly, rats that lacked control over food pellets preferred more alcohol than rats with control over food pellets. A two-way mixed analysis of variance revealed a reliable groups effect, F(1,8)= 7.39, p<0.01; but no reliable trials or groups by trials interaction effects. A similar analysis of total fluid consumption revealed no reliable groups, or groups by trials interaction effects. A separate analysis of water and alcohol drinking is presented in Table 1. As this table reveals, the yoked group drank significant levels of ethanol averaging 9.14 g/kg body weight. This is a level comparable to that observed by Falk and his colleagues (5) and a level that has been associated with signs of alcohol withdrawal symptoms when the alcohol was removed. The excess drinking is specific to the ethanol bottle since there were no reliable differences in water drinking. Not unexpectedly, the yoked rats tended to weigh more (terminal weight) than the control rats at the end of the experiment since not only did they eat the same amount of food as the control rats, but they also had additional calories from their increased ethanol drinking. Our unsystematic observations revealed that under these feeding conditions rats with control tended to space feedings at fourhour intervals and all animals tended to drink alcohol during these feeding periods. This observation is consistent with those of Falk and Samson (5) who demonstrated that alcohol drinking increased during feedings. EXPERIMENT 2: AVERSIVE CONTROL The first experiment showed that rats with lack of control over
CONTROL AND ALCOHOL DRINKING
appetitive events preferred alcohol more than rats with control. The yoked procedure insured that this difference was not due to the pattern of food presentations since food presentations were identical for both groups. Rather, the results suggest that lacking control over important environmental events increases alcohol preference. However, although rats were paired for initial weight and received equivalent amounts of food, it is still possible that yoked rats drank alcohol for its caloric value. If a rat with control was hungry, he could lever press for food, whereas a yoked animal had free access to alcohol only. In addition, the rats may have increased preference for the alcohol solution because it was sweetened with saccharin. Thus, yoked rats may have drunk the alcohol solution for its specific caloric properties, its sweetened taste, or some pharmacologic effect of alcohol. If alcohol drinking is influenced by controllability per se, then it should be possible to modify alcohol consumption using nonappetitive reinforcers and unsweetened alcohol solutions. So, for example, rats exposed to uncontrollable foot shocks should drink more unsweetened alcohol than rats with control over footshock. Since this species of rats drinks very little unsweetened 10% alcohol solutions, one can insure that alcohol is sampled by gradually increasing the alcohol concentration. These procedural changes help to eliminate confounds due to the caloric value of alcohol or the sweetness of the alcohol solution used in Experiment 1. In addition, this experiment attempts to generalize the results of Experiment 1 across type of reinforcer (i.e., food presentations versus shock termination). METHOD
Subjects Subjects were 12 male Sprague-Dawley rats obtained from Holtzman Co., Madison, WI. The rats were 80 days old at the start of the experiment and were individually housed and maintained in a constant light environment, with food, water, and ethanol freely available in the home cage. The subjects were nonsystematically assigned to one of two shock conditions: yoked inescapable or escapable, N = 6/group. Apparatus Escapable and inescapable shock treatments were carried out in two identical shuttleboxes, 47.0 cm long, 20.4 cm wide, and 19.7 cm high. The walls were constructed of stainless steel with a ceiling of clear acrylic plastic. The floor consisted of stainless steel grid bars, 0.4 cm in diameter, 1.9 cm apart. Each chamber was divided into two identical sections by 0.64 cm metal divider with a rounded archway 7.8 cm high and 5.8 cm wide cut out of the bottom. The chambers were illuminated by a 75 W bulb mounted on the inside of the sound attenuating shell which enclosed the chamber. An 0.8 mA scrambled electric shock was delivered through the grid floor and sides of the shuttleboxes by a constant current shock source consisting of a 600 V AC transformer and a limiting resistor. Food, water, and alcohol were freely available in the home cage of the subjects. As in Experiment 1, water and alcohol were available from fluid bottles that hung outside the home cage with spouts that protruded about 2.0 cm into the home cage. This method of obtaining fluid minimized spillage. Indeed, throughout the course of the experiment, no spillage was observed. Procedure Rats received shock experience on Days 1, 3, and 5. On Day 1, the escape group received 50 shock trials in which a single shuttle response terminated shock. On Days 3 and 5, the rats were required to shuttle twice to terminate shock. The increase in
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FIG. 2. Mean ethanol preference for rats with control over shock escape and rats which receivedyoked shock deliveriesacross days with increasing ethanol concentrations.
response requirement to an FR-2 following the first day of shock has been typically used in helplessness experiments to insure sufficient shock experience, as the control rats become proficient at learning to escape shock [see Volpicelli et al. (18)]. Failure to terminate shock on any trial resulted in 30 seconds of shock. Shock trials were delivered on a variable time (VT) 60-second schedule (range, 10-110 seconds). Yoked inescapable shock animals were paired with escape subjects and received shocks identical to their escape partners. Immediately following shock experience, rats were returned to their home cages where water and the alcohol solutions were freely available. Thus alcohol was not available during the shock experiences. For both the Yoked and Escape groups, a 2.5% ethanol (V/V) solution was available during the two days following the first shock experience. A 5% ethanol solution was used for the two days following the second shock experience, and a 10% ethanol solution was available for the remainder of the experiment. Throughout the experiment, bottle positions were alternated and weighed daily. RESULTS
AND DISCUSSION
Figure 2 shows alcohol preference for the 2.5%, the 5%, and the 10% alcohol solutions. This figure reveals that rats which received inescapable shock preferred alcohol more than rats which received escapable shock. A two-way mixed analysis of variance revealed a reliable groups effect, F(1,10)=9.61, p<0.025; a reliable decrease in alcohol preference across days as the alcohol concentration increased, F(9,90) = 5.84, p<0.001. The groups by days interaction was not significant, F(9,90)= 1.26. As shown in Table 2, mean water drinking was reliably less in the yoked group while alcohol drinking was reliably greater. Thus the increased alcohol preference reflects absolute differences in alcohol drinking and not differences in total fluid consumption. The table also shows that the groups did not differ in terminal body weight. This experiment shows that when access to alcohol is given in the home cage following shock experience, degree of control over the shock dramatically affects alcohol drinking. The results of Experiment 2, then, parallel Experiment 1 in demonstrating that rats without control prefer significantlymore alcohol than rats with control even in a setting in which food is freely available. Thus, it seems clear that lack of control is the critical factor influencing alcohol drinking rather than any caloric property of alcohol.
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VOLPICELLI AND ULM
TABLE 2 MEANS, STANDARD ERRORS, AND t-TESTS FOR WATER, ETHANOL, AND TERMINAL WEIGHT FOR THE ESCAPE AND YOKED CONDITIONS OF EXPERIMENT 2
Water (ml) Ethanol (g/kg) Terminal Weight (g)
Escape Group
Yoked Group
t-test
26.0 (1.87) 1.58 (0.22) 388 (2.87)
15.6 (2.69) 3.40 (0.26) 399 (3.07)
2.62, p<0.05 4.37 p<0.01 n.s.
GENERAL DISCUSSION Rats which lack control over either appetitive or aversive events prefer substantially more alcohol than animals with control. This effect was not due to any general increase in drinking behavior because the yoked animals in neither experiment drink more total fluid than the control animals. It is possible that uncontrollability per se increases preference for alcohol not because of its intoxicating properties but because of the higher caloric value of the alcohol solution. This interpretation seems unlikely to us but experiments comparing alcohol to isocaloric nonintoxicating solutions could control for this possibility. Clearly, these two experiments implicate lack of control as an important variable in alcohol preference. The results are consistent with previous research which shows that during intermittent delivery of food pellets (5) or following uncontrollable electric
footshock, (1, 10, 17) rats drink substantial amounts of alcohol. Furthermore, the magnitude of alcohol drinking is influenced by the degree to which rats can control the reinforcer. It is not clear why yoked animals drank more alcohol. It can be argued that rats which lack control over environmental events are exposed to more " s t r e s s " than rats which have control. Since it has been suggested that alcohol reduces tension (3) or dampens stress (13), perhaps the yoked animals used alcohol to attenuate stress. This explanation is plausible for the data presented here. The results of the shock experiment (Experiment 2) are also consistent with the hypothesis that rats drink alcohol to stimulate endorphin activity. Experience with uncontrollable shock increases endorphinergic activity but presentation of identical shocks that can be controlled by an escape response does not (8). Therefore, Volpicelli (16) has argued that just as chronic opiate use can lead to rebound deficiencies in opiate receptor activity, following uncontrollable shock, a deficiency in opiate activity exists. This deficiency can be compensated for by alcohol drinking. The Endorphin Compensation Hypothesis, however, does not easily explain the results of the food experiment (Experiment 1). In general, the results of these two experiments clearly show that control over important environmental events influences alcohol preference. Relative to rats which control shock termination or food presentations, rats which lack control have increased alcohol preference. ACKNOWLEDGEMENT This work is supported in part by the NIDA Addiction Research Center, grant No. DA05186.
REFERENCES 1. Anisman, H.; Waller, T. G. Effects of inescapable shock and shock-produced conflict on self selection of alcohol in rats. Pharmacol. Biochem. Behav. 2:27-33; 1974. 2. Beckman; L. J. Perceived antecedents and effects of alcohol consumption in women. J. Stud. Alcohol 41:518-530; 1980. 3. Cappell, H.; Greeley, J. Alcohol and tension reduction: An update on research and theory. In: Blaine, H. T.; Leonard, K. E., eds. Psychological theories of drinking and alcoholism. New York: The Guilford Press; 1987:15-50. 4. Engberg, L. A.; Goldberg, L.; Volpicelli, J. R. Transfer of helplessness from an appetitive to an aversive situation. Bull. Psychon. Soc. 10:445; 1975. 5. Falk, J. L.; Samson, H. H. Schedule induced physical dependence on ethanol. Psychopharmacol. Rev. 127:449--464; 1976. 6. Goodkin, F. Rats learn the relationship between responding and environmental events: An expansion of the learned helplessness hypothesis. Learn. Motiv. 7:382-394; 1976. 7. Landenslager, M. L.; Ryan, S. M.; Drugan, R. C.; Hyson, R. L.; Maier, S. F. Coping and immunosuppression: Inescapable but not escapable shock suppresses lymphocyte proliferation. Science 221: 568-570; 1983. 8. Maier, S. F.; Drugan, R. C.; Grau, J. W. Controllability, coping behavior, and stress-induced analgesia in the rat. Pain 12:47-56; 1982. 9. Maler, S. F.; Seligman, M. E. P. Learned helplessness: Theory and evidence. J. Exp. Psychol. [Gen.] 105:3-46; 1976.
10. Mills, K. C.; Bean, J. W. Shock-induced ethanol consumption in rats. Pharmacol. Biochem. Behav. 6:107-115; 1978. 11. Noel, N. E.; Lisman, S. A. Alcohol consumption by college women following exposure to unsolvable problems: Learned helplessness or stress-induced drinking? Behav. Res. Ther. 18:429-440; 1980. 12. Rossier, J.; French, E. D.; Rivier, C.; Ling, M.; Guillemin, R.; Bloom, F. E. Foot-shock induced stress increases beta-endorphin levels in blood but not brain. Nature 270:618-620; 1977. 13. Sher, K. J. Stress response dampening. In: Blaine, H. T.; Leonard, K. E., eds. Psychological theories of drinking and alcoholism. New York: The Guilford Press; 1987:227-264. 14. Swenson, R. M.; Vogel, W. H. Plasma catecholamines as well as brain catecholamines change during coping in rats exposed to stressful shock. Pharmacol. Biochem. Behav. 18:689-693; 1983. 15. Visintainer, M. A.; Volpicelli, J. R.; Seligman, M. E. P. Tumor rejection in rats after inescapable or escapable shock. Science 216: 437-439; 1982. 16. Volpicelli, J. R. Uncontrollable events and alcohol drinking. Br. J. Addict. 82:381-392; 1987. 17. Volpicelli, J. R.; Tiven, J.; Kimmel, S. C. The relationship between tension reduction and ethanol consumption in rats. Physiol. Psychol. 10:114---116; 1982. 18. Volpicelli, J. R.; Ulm, R. R.; Altenor, A.; Seligman, M. E. P. Learned mastery in the rat. Learn. Motiv. 14:204--222; 1983. 19. Weiss, J. M. Effects of coping responses on stress. J. Comp. Physiol. Psychol. 65:251-260; 1968.
0741-8329/90$3.00 + .00
The Influence Of Control Over Appetitive and Aversive Events on Alcohol Preference in Rats J O S E P H R. V O L P I C E L L I 1
Departments of Psychiatry and Psychology, University of Pennsylvania, Philadelphia, PA 19104 AND R O N A L D R. U L M
Department of Psychology, Salisbury State University, Salisbury, MD 21801 Received 5 July 1988; Accepted 29 July 1989
VOLPICEIJ.I, J. R. AND R. R. ULM. The influence of control over appetitive and aversive events on alcoholpreference in rats. ALCOHOL 7(2) 133-136, 1990.-- The effect of control of food reinforcement or shock termination on alcohol drinking was examined in two experiments. In the In'st experiment, rats unable to control the delivery of food pellets preferred alcohol more than rats which had control over food. Similarly, in the second experiment, rats unable to control electric footshoek termination preferred alcohol more than rats which could escape shock. These results showed that the psychological dimension of control over environmental events influences alcohol preference in rats. Stress
Alcohol self-selection
Rats
Uncontrollable shock
ANIMALS and humans lacking control over aversive events exhibit a variety of behavioral and physiological changes which have been commonly referred to as helplessness effects (9). These experiments always use the yoked control procedure. This procedure involves matching pairs of subjects such that all physical stimuli are held constant, but one subject controls the presentation or termination of the important stimulus event. For example, in the typical helplessness experiment, shock presentations are identical for each pair of rats, but one of the rats can escape from shock (master rat) while shock termination occurs at the same time regardless of the behavior of its yoked partner (helpless rat). In this way, only the controllability of the important stimulus event is varied while the physical properties of the event are held constant. Thus, the duration, intensity, and pattern of shocks is identical within each pair. Using this yoked control procedure, Maier and Seligman (9) have demonstrated that uncontrollably shocked rats are more passive in new situations than rats exposed to equivalent amounts of controllable shock. Others have shown that uncontrollable shock leads to immunosuppression (7), gastric ulceration (19), decreased resistance to a tumor challenge (15), higher catecholamine and corticosterone levels (14), and higher 13-endorphin levels
Uncontrollable food
Tension reduction hypothesis
in peripheral blood (12). In the few studies which have systematically examined the influence of controllability on appetitive events, similar behavioral helplessness effects have been observed. Goodkin et al. (6) found that, following uncontrollable food pellets, rats were slower to learn a new response to obtain food reward and were more passive in a novel shock escape task than rats exposed to equivalent amounts of controllable food. Similarly, Engberg et al. (4) found that, following uncontrollable food pellets, rats were also slower to escape in a new shock escape task. There is some indication that the psychological dimension of control over environmental events may be related to alcohol drinking. Human alcoholics, for example, report feelings of lack of control over alcohol drinking as well as other aspects of their lives (2). However, there is little systematic research that investigates this relationship. One exception is a study that showed increased alcohol drinking following unsolvable problems in female social drinkers (11). Alcohol per se may lead to increased feelings of lack of control, or conversely, uncontrollable events may lead to alcoholism. The present experiments attempt to clarify this issue by systematically assessing the effects of controllability on alcohol drinking in rats.
~Requests for reprints should be addressed to Joseph R. Volpicelli, M.D., Ph.D., Addiction Research Center, 3910 Chestnut St., University of Pennsylvania, Philadelphia, PA 19104.
133
134
VOLPICELLI AND ULM
EXPERIMENT 1: APPETITIVE CONTROL There have been several attempts to elicit excessive alcohol drinking in rats using appetitive events. For example, Falk and Samson (5), found that food-deprived rats with access to a 5% alcohol solution drank large amounts of alcohol when a food pellet was delivered uncontrollably about once every two minutes. This procedure has been termed scheduled-induced polydipsia and it has been used to induce animals to drink an excessive amount of many fluids including water. Since the controllability dimension was not systematically varied, however, it is not clear from this research whether rats drank alcohol, 1) for some reinforcing pharmacological effect of alcohol related to the lack of control over food pellets, 2) because drinking is nonspecifically directed at alcohol because it is the only fluid available or 3) to compensate for their restricted caloric schedule. Therefore, our first experiment systematically investigated the effects of controllability over food pellets using the yoked control procedure. Since alcohol preference is examined in a two-bottle test with both alcohol and water continuously available, and rats receive equivalent amounts of food, differences between the yoked and control subjects can be attributed to the psychological effects of lack of control over food. METHOD
Subjects Subjects were 10 male Sprague-Dawley rats (N=5/group) obtained from Holtzman Co., Madison, WI. Rats were obtained at 60 days of age and were individually housed and raised in a 14 hr light-10 hr dark environment. During the first seven days subjects were gradually reduced to 80% body weight and then paired according to weight and placed in operant chambers, with control versus yoked assignment randomly determined.
Apparatus Subjects lived in a modified Skinner box with a lever mounted on the front of the chamber and two graduated cylinders mounted at the rear of the chamber so that both alcohol and water were freely available at all times. Rats obtained fluid by licking narrow metal drinking spouts that protruded 2 cm into the cage. This technique was used to eliminate the spillage that can occur with other types of drinking tubes.
Procedure Following assignment into the yoked or control groups, rats were placed in operant chambers for the next 28 days. Water and 10% alcohol sweetened with 0.25% sodium saccharin was freely available to all subjects. Food pellets (45 mg Noyes pellets) were delivered to both the control and its yoked partner when the control rat pressed the lever. On day 1, each lever-press resulted in a food pellet and on subsequent days lever-pressing was reinforced on a VI-60 second schedule (range 10 to 120 sec). Since subjects in both groups ate the pellets immediately when it was delivered, the only difference between the two groups was that the control group could control food presentations by lever-pressing while the yoked rats had no control over food presentations. This appetitive schedule control feeding was in effect 24 hr/day. Dally measurements of the weight and fluid consumption of each rat were made and followed by placing a fresh supply of water or alcohol into the graduated cylinders. To avoid position biases the fluid cylinders were rotated daily. RESULTS AND DISCUSSION
In order to control for difference in total fluid consumption, the
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FIG. 1. Mean ethanol preference for rats with control over food pellets and rats which received yoked pellet presentations across 14 blocks of two-day averages.
TABLE
1
MEANS, STANDARD ERRORS, AND t-TESTS FOR WATER, ETHANOL, AND TERMINAL WEIGHT FOR THE CONTROL AND YOKED CONDITIONS OF EXPERIMENT 1
Water (ml) Ethanol (g/kg) Terminal Weight (g)
Control Group
Yoked Group
t-test
19.34 (2.19) 5.08 (0.89) 409 (10.00)
13.5 (2.09) 9.14 (0.69) 429 (8.17)
n.s. 3.21, p<0.03 n.s.
percent alcohol preference was calculated by dividing the volume of alcohol consumed by the total fluid consumed and multiplying the result by 100. Figure 1 shows the average percent alcohol preference over 14 blocks of two-day averages for the control and yoked groups. Clearly, rats that lacked control over food pellets preferred more alcohol than rats with control over food pellets. A two-way mixed analysis of variance revealed a reliable groups effect, F(1,8)= 7.39, p<0.01; but no reliable trials or groups by trials interaction effects. A similar analysis of total fluid consumption revealed no reliable groups, or groups by trials interaction effects. A separate analysis of water and alcohol drinking is presented in Table 1. As this table reveals, the yoked group drank significant levels of ethanol averaging 9.14 g/kg body weight. This is a level comparable to that observed by Falk and his colleagues (5) and a level that has been associated with signs of alcohol withdrawal symptoms when the alcohol was removed. The excess drinking is specific to the ethanol bottle since there were no reliable differences in water drinking. Not unexpectedly, the yoked rats tended to weigh more (terminal weight) than the control rats at the end of the experiment since not only did they eat the same amount of food as the control rats, but they also had additional calories from their increased ethanol drinking. Our unsystematic observations revealed that under these feeding conditions rats with control tended to space feedings at fourhour intervals and all animals tended to drink alcohol during these feeding periods. This observation is consistent with those of Falk and Samson (5) who demonstrated that alcohol drinking increased during feedings. EXPERIMENT 2: AVERSIVE CONTROL The first experiment showed that rats with lack of control over
CONTROL AND ALCOHOL DRINKING
appetitive events preferred alcohol more than rats with control. The yoked procedure insured that this difference was not due to the pattern of food presentations since food presentations were identical for both groups. Rather, the results suggest that lacking control over important environmental events increases alcohol preference. However, although rats were paired for initial weight and received equivalent amounts of food, it is still possible that yoked rats drank alcohol for its caloric value. If a rat with control was hungry, he could lever press for food, whereas a yoked animal had free access to alcohol only. In addition, the rats may have increased preference for the alcohol solution because it was sweetened with saccharin. Thus, yoked rats may have drunk the alcohol solution for its specific caloric properties, its sweetened taste, or some pharmacologic effect of alcohol. If alcohol drinking is influenced by controllability per se, then it should be possible to modify alcohol consumption using nonappetitive reinforcers and unsweetened alcohol solutions. So, for example, rats exposed to uncontrollable foot shocks should drink more unsweetened alcohol than rats with control over footshock. Since this species of rats drinks very little unsweetened 10% alcohol solutions, one can insure that alcohol is sampled by gradually increasing the alcohol concentration. These procedural changes help to eliminate confounds due to the caloric value of alcohol or the sweetness of the alcohol solution used in Experiment 1. In addition, this experiment attempts to generalize the results of Experiment 1 across type of reinforcer (i.e., food presentations versus shock termination). METHOD
Subjects Subjects were 12 male Sprague-Dawley rats obtained from Holtzman Co., Madison, WI. The rats were 80 days old at the start of the experiment and were individually housed and maintained in a constant light environment, with food, water, and ethanol freely available in the home cage. The subjects were nonsystematically assigned to one of two shock conditions: yoked inescapable or escapable, N = 6/group. Apparatus Escapable and inescapable shock treatments were carried out in two identical shuttleboxes, 47.0 cm long, 20.4 cm wide, and 19.7 cm high. The walls were constructed of stainless steel with a ceiling of clear acrylic plastic. The floor consisted of stainless steel grid bars, 0.4 cm in diameter, 1.9 cm apart. Each chamber was divided into two identical sections by 0.64 cm metal divider with a rounded archway 7.8 cm high and 5.8 cm wide cut out of the bottom. The chambers were illuminated by a 75 W bulb mounted on the inside of the sound attenuating shell which enclosed the chamber. An 0.8 mA scrambled electric shock was delivered through the grid floor and sides of the shuttleboxes by a constant current shock source consisting of a 600 V AC transformer and a limiting resistor. Food, water, and alcohol were freely available in the home cage of the subjects. As in Experiment 1, water and alcohol were available from fluid bottles that hung outside the home cage with spouts that protruded about 2.0 cm into the home cage. This method of obtaining fluid minimized spillage. Indeed, throughout the course of the experiment, no spillage was observed. Procedure Rats received shock experience on Days 1, 3, and 5. On Day 1, the escape group received 50 shock trials in which a single shuttle response terminated shock. On Days 3 and 5, the rats were required to shuttle twice to terminate shock. The increase in
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FIG. 2. Mean ethanol preference for rats with control over shock escape and rats which receivedyoked shock deliveriesacross days with increasing ethanol concentrations.
response requirement to an FR-2 following the first day of shock has been typically used in helplessness experiments to insure sufficient shock experience, as the control rats become proficient at learning to escape shock [see Volpicelli et al. (18)]. Failure to terminate shock on any trial resulted in 30 seconds of shock. Shock trials were delivered on a variable time (VT) 60-second schedule (range, 10-110 seconds). Yoked inescapable shock animals were paired with escape subjects and received shocks identical to their escape partners. Immediately following shock experience, rats were returned to their home cages where water and the alcohol solutions were freely available. Thus alcohol was not available during the shock experiences. For both the Yoked and Escape groups, a 2.5% ethanol (V/V) solution was available during the two days following the first shock experience. A 5% ethanol solution was used for the two days following the second shock experience, and a 10% ethanol solution was available for the remainder of the experiment. Throughout the experiment, bottle positions were alternated and weighed daily. RESULTS
AND DISCUSSION
Figure 2 shows alcohol preference for the 2.5%, the 5%, and the 10% alcohol solutions. This figure reveals that rats which received inescapable shock preferred alcohol more than rats which received escapable shock. A two-way mixed analysis of variance revealed a reliable groups effect, F(1,10)=9.61, p<0.025; a reliable decrease in alcohol preference across days as the alcohol concentration increased, F(9,90) = 5.84, p<0.001. The groups by days interaction was not significant, F(9,90)= 1.26. As shown in Table 2, mean water drinking was reliably less in the yoked group while alcohol drinking was reliably greater. Thus the increased alcohol preference reflects absolute differences in alcohol drinking and not differences in total fluid consumption. The table also shows that the groups did not differ in terminal body weight. This experiment shows that when access to alcohol is given in the home cage following shock experience, degree of control over the shock dramatically affects alcohol drinking. The results of Experiment 2, then, parallel Experiment 1 in demonstrating that rats without control prefer significantlymore alcohol than rats with control even in a setting in which food is freely available. Thus, it seems clear that lack of control is the critical factor influencing alcohol drinking rather than any caloric property of alcohol.
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TABLE 2 MEANS, STANDARD ERRORS, AND t-TESTS FOR WATER, ETHANOL, AND TERMINAL WEIGHT FOR THE ESCAPE AND YOKED CONDITIONS OF EXPERIMENT 2
Water (ml) Ethanol (g/kg) Terminal Weight (g)
Escape Group
Yoked Group
t-test
26.0 (1.87) 1.58 (0.22) 388 (2.87)
15.6 (2.69) 3.40 (0.26) 399 (3.07)
2.62, p<0.05 4.37 p<0.01 n.s.
GENERAL DISCUSSION Rats which lack control over either appetitive or aversive events prefer substantially more alcohol than animals with control. This effect was not due to any general increase in drinking behavior because the yoked animals in neither experiment drink more total fluid than the control animals. It is possible that uncontrollability per se increases preference for alcohol not because of its intoxicating properties but because of the higher caloric value of the alcohol solution. This interpretation seems unlikely to us but experiments comparing alcohol to isocaloric nonintoxicating solutions could control for this possibility. Clearly, these two experiments implicate lack of control as an important variable in alcohol preference. The results are consistent with previous research which shows that during intermittent delivery of food pellets (5) or following uncontrollable electric
footshock, (1, 10, 17) rats drink substantial amounts of alcohol. Furthermore, the magnitude of alcohol drinking is influenced by the degree to which rats can control the reinforcer. It is not clear why yoked animals drank more alcohol. It can be argued that rats which lack control over environmental events are exposed to more " s t r e s s " than rats which have control. Since it has been suggested that alcohol reduces tension (3) or dampens stress (13), perhaps the yoked animals used alcohol to attenuate stress. This explanation is plausible for the data presented here. The results of the shock experiment (Experiment 2) are also consistent with the hypothesis that rats drink alcohol to stimulate endorphin activity. Experience with uncontrollable shock increases endorphinergic activity but presentation of identical shocks that can be controlled by an escape response does not (8). Therefore, Volpicelli (16) has argued that just as chronic opiate use can lead to rebound deficiencies in opiate receptor activity, following uncontrollable shock, a deficiency in opiate activity exists. This deficiency can be compensated for by alcohol drinking. The Endorphin Compensation Hypothesis, however, does not easily explain the results of the food experiment (Experiment 1). In general, the results of these two experiments clearly show that control over important environmental events influences alcohol preference. Relative to rats which control shock termination or food presentations, rats which lack control have increased alcohol preference. ACKNOWLEDGEMENT This work is supported in part by the NIDA Addiction Research Center, grant No. DA05186.
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