Department of Psychology and Center of Alcohol Studies, Rutgers University, New Brunswick, NJ 08903, USA
Received 11 February 2002; in revised form 26 April 2002; accepted 10 May 2002
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ABSTRACT |
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INTRODUCTION |
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The present experiment asks if drinking may be induced in rats by Pavlovian autoshaping procedures, and, if so, the degree to which the drinking of a 6% ethanol solution may be acquired and maintained. The traditional rat autoshaping apparatus was modified by replacing the retractable lever CS with a retractable sipper tube CS that was attached to a Plexiglas bottle filled with solution. The sipper CS was inserted for 5 s and then retracted immediately prior to the response-independent delivery of the food US. After repeated sipper CSfood US pairings, the autoshaping model predicts that rats will acquire the Pavlovian autoshaping CR, and this will be revealed by the development of consummatory-like responding directed at the sipper CS. Thus, repeated pairings of the sipper CS with the food US is expected to induce autoshaping of drinking of the solution in the sipper CS.
Two recent studies have employed these autoshaping procedures in conjunction with saccharin fading procedures to induce sipper CS-directed drinking of 6% ethanol (v/v) in food-deprived rats (Tomie et al., 2002a,b
). The purpose of the present study is to assess the degree to which the autoshaping procedures employed by Tomie et al. (2002a)
would also induce drinking of water from the sipper CS. This is an important consideration, as the drinking of 6% ethanol observed by Tomie et al. (2002a)
may be due to the caloric value of the 6% ethanol solution, which would not be a factor when the sipper CS contained tap water. The Pavlovian autoshaping model predicts that the water control group will drink the solution in the sipper CS, even when the sipper CS contains a water solution with no caloric value.
The present study was also designed to assess the durability of the drinking effects established by Pavlovian autoshaping procedures. Groups of rats provided with 6% ethanol (Ethanol group) or tap water (Water group) in the sipper CS were evaluated for changes in sipper CS-directed drinking across a 27-day retention interval. Once acquired, Pavlovian CRs are typically maintained across long retention intervals (Mackintosh, 1974); therefore, the drinking established by these autoshaping procedures is expected to be durable. Finally, the present study will also assess the effects of increasing the mean duration of time that the rat has access to the sipper CS on each autoshaping trial on the rate of drinking from the sipper CS. Autoshaping investigators have reported that the rate of performance of autoshaping CRs declines with longer CS durations (Gibbon and Balsam, 1981
; Jenkins et al., 1981
; Killeen, 1984
); therefore, the autoshaping model predicts that increasing the sipper CS duration will decrease the rate of drinking (millilitres of fluid consumed per second of CS duration), and this effect should be observed in both the Ethanol and Water groups.
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MATERIALS AND METHODS |
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Apparatus
Autoshaping chambers were four Plexiglas cubicles (24 x 24 x 26 cm) with a stainless steel grid floor all enclosed in sound-attenuating, ventilated outer casings. One house light (GE 1821) was mounted directly above the operant chamber on the ceiling of the outer hull. The front panel of each chamber was equipped with a retractable stainless steel sipper tube containing a stainless steel ball-bearing with an inserted rubber stopper holding the fluid in a 50 ml Plexiglas graduated tube (model 58320; Kimble-Kontes, Vineland, NJ, USA). The Plexiglas tube was mounted on a mechanical bottle insertion mechanism (BCS Machine, South Plainfield, NJ, USA), which inserted the stainless steel sipper tube 3.5 cm above the grid floor and 3 cm to the left of the centreline. The bottle insertion mechanism moved the sipper tube a total of 2.75 cm from fully retracted to fully inserted. In the fully retracted position, the sipper tube was 2.0 cm removed from the chamber. A contact lickometer recorded licks (model ENV-250; Med Associates, St Albans, VT, USA). A metal food pellet receptacle was mounted 3 cm to the right of the centreline, and 4 cm above the floor. The food pellet dispenser (model PDC/PPD, BRS/LVE) delivered 45 mg food pellets (#F0165, BioServ, Frenchtown, NJ, USA). Masking noise (88 dB, linear scale) was provided by the operation of ventilating exhaust fans mounted on the outer hull. IBM PCs controlled session events.
Drugs
Bulk ethanol (95%) was obtained from Rutgers University Chemical Stores. Saccharin sodium was obtained from Sigma Chemical Co., St Louis, MO, USA.
Autoshaping procedure
Rats were run 5 days per week and received two autoshaping sessions per day. Morning sessions were conducted between 09:00 and 12:00, whereas afternoon sessions were conducted between 13:00 and 16:00. Prior to each autoshaping session, rats were weighed and then immediately placed in the autoshaping chamber. Eight rats were randomly assigned to the Ethanol group, and eight rats were assigned to the Water group. For both groups, the sipper tube (CS) was inserted for 5 s, followed immediately by the response-independent operation of the pellet dispenser (US). For both the Ethanol and Water groups, the delivery of the food pellet US occurred regardless of whether the subject contacted the sipper CS. Both groups received a total of 25 trials per autoshaping session. The mean inter-trial interval (ITI) duration was 60 s, with a minimum of 45 s and a maximum of 75 s. The session duration was 30 min. Volume of fluid consumed (ml) during each autoshaping session was determined by recording the volume in the tube immediately before and after each session.
For the first 19 days of autoshaping, the Ethanol group received 6% ethanol in 0.1% saccharin solution. During days 2031, the Ethanol group received 6% ethanol in 0.07% saccharin solution. During days 3235, the Ethanol group received 6% ethanol in 0.035% saccharin solution. During days 3640, the Ethanol group received 6% ethanol in 0% saccharin (tap water) solution. The water group received identical training (i.e. the same saccharin fading procedure) with 0% ethanol (tap water) rather than 6% ethanol.
Following the 40th day, autoshaping procedures were suspended for the next 27 days (4167). All rats were placed on free-feed for 20 days, and during days 6067 all rats were food-deprived to 8085% of their ad libitum weights. Following the completion of the 27-day retention interval, the effects of increasing the duration of access to the sipper CS were evaluated. During days 6878, all rats received 11 days of autoshaping procedures identical to those given on day 40, with the CS duration of 5 s. During days 7988, the CS duration was 7.5 s. During days 8993, the CS duration was 10 s, and during days 94115, the CS duration was 15 s.
Blood-ethanol assay
Immediately after the second autoshaping session of day 103, each rat was manually restrained and a scalpel was used to remove the last 510 mm of the tip of the tail. Samples of tail blood were collected to assay blood ethanol. For all rats, latency to collect the tail blood samples following the incision was 12 min. Tail blood samples were assayed for blood-ethanol levels using Sigma Diagnostics Enzymatic Alcohol Assay Kit (Product #332-C).
Statistics
For each subject, for each autoshaping session, the following data were obtained: ml of fluid consumed, total number of sipper tube licks, body weight, and g/kg of ethanol consumed. For each group, effects of autoshaping sessions on mean ml of fluid consumed, mean number of licks, and mean g/kg were assessed by one-way repeated-measures analysis of variance using ANOVA (Systat). For all of these measures, for each subject in each group we derived the mean of the last 4 days of autoshaping for each saccharin concentration (0.1, 0.07, 0.035, 0.0%) and each CS duration (5, 7.5, 10, 15 s). The mean of the last 4 days of training under each condition provided a stable estimate of asymptotic drinking for each group that did not vary by >10% between consecutive days. Effects of groups and saccharin concentration and effects of groups and CS duration were assessed by two-way repeated-measures multivariate analysis of variance using MANOVA (Systat). The forms of the functions (linear or quadratic) relating drinking to CS duration were evaluated using orthogonal polynomial contrasts (Systat). Statistical adjustments were made to maintain family-wise P values at an alpha level of 0.05 by dividing 0.05 by the number of effects reported in the family-wise analysis.
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RESULTS |
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Effects of the retention interval
The levels of drinking for both the Ethanol and Water groups were virtually unaffected by the 27-day retention interval, suggesting robust long-term retention of sipper CS-directed autoshaping CRs. The maintenance of autoshaping CRs across the retention interval was evaluated for each group in two ways. Comparing a groups mean drinking during the last 4 days immediately prior to the retention interval (days 3740) to that groups mean drinking during the first day immediately following the retention interval (day 68) allows for assessment of the immediate impact of the retention interval on drinking. The longer-term maintenance of post-retention interval drinking was assessed by comparing a groups mean drinking during the last 4 days immediately prior to the retention interval (days 3740) to that groups mean drinking during the first 4 days immediately following the retention interval (days 6871).
The results are shown in Fig. 2. For the Ethanol group, analysis of the effect of the retention interval on mean ml of 6% ethanol solution consumed during the first day following the retention interval (days 3740 vs day 68) revealed no significant main effect of the retention interval (F < 1). A similar analysis for the Water group also revealed no significant main effect of the retention interval (F < 1). For the Ethanol group, analysis of the effects of the retention interval on mean ml of 6% ethanol solution consumed during the first 4 days following the retention interval (days 3740 vs days 6871) also revealed no significant main effect of the retention interval (F < 1). In addition, a similar analysis for the Water group also revealed no significant main effect of the retention interval (F < 1).
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For the Ethanol group, the function relating g/kg ethanol consumed per day to CS duration was biphasic in form. Analysis revealed a significant main effect of CS duration [F(3,21) = 13.004, P = 0.000] (Fig. 4, upper panel), and orthogonal polynomial contrasts revealed a significant quadratic component [F(1,7) = 21.914, P = 0.002]. Pairwise comparison of g/kg ethanol consumed per day at the 10 s CS duration vs the 15 s CS duration revealed that the difference was significant [F(1,15) = 7.053, P = 0.018]. When these data were expressed as rate of drinking, the function relating g/kg ethanol consumed per second of CS duration was descending and monotonic in form (Fig. 4
, lower panel). Analysis revealed a significant main effect of CS duration [F(3,21) = 15.481, P = 0.000] and orthogonal polynomial contrasts revealed a significant linear component [F(1,7) = 18.281, P = 0.004].
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DISCUSSION |
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This is the first report of autoshaping of drinking of water. The data of the Water group show that these Pavlovian autoshaping procedures induced drinking when the sipper CS contained tap water, even though the rats were maintained in their home cages with unrestricted access to water, making it unlikely that the rats drank to alleviate a condition of fluid deprivation. In addition, drinking in the Water group cannot be attributed to foraging for calories by hungry rats, as water has no caloric value. The autoshaping hypothesis suggests that the drinking of water is due to the reflexive and involuntary expression of sipper CS-directed autoshaping CR performance.
The Ethanol group drank more than the Water group, and this difference was evident at all saccharin concentrations and was most pronounced when the sipper CS contained no saccharin. It is possible that the elevated drinking in the Ethanol group is due to differences in the caloric content of the solutions offered to the food-deprived rats (Heyman, 1993, 1997
; Samson et al., 2000
). An alternative account of the enhanced drinking in the Ethanol group was based on the effects of ethanol on autoshaping CR performance. There is evidence that pre-session intraperitoneal (i.p.) injections of ethanol enhance performance of lever-press autoshaping CRs in rats receiving lever CSfood US pairings (Tomie et al., 1998
). Moreover, ethanols effects were dose-dependent, such that increasing i.p. doses of ethanol up to 1.0 g/kg were associated with higher levels of autoshaping CR performance. This suggests that, in the present study, the drinking of ethanol would be expected to augment autoshaping CR performance, resulting in more sipper CS-directed autoshaping CRs and more drinking in the Ethanol group than the Water group. This analysis speaks to the issue of why ethanol intake is likely to be exaggerated within a drinking episode. If ethanols pharmacological effect is to augment autoshaping of ethanol drinking, then the ethanolautoshaping interaction provides a positive feedback loop mechanism that will promote the exaggerated expression of ethanol intake (Tomie et al., 2002a
).
These data provide evidence of long-term retention of sipper CS-directed drinking, suggesting that drinking established by autoshaping procedures is quite durable. Relative to the pre-retention baseline, there were virtually no effects of the 27-day retention interval on mean ml of fluid consumed for the Ethanol group, and this was true on the first day following the retention interval as well as on the first 4 days following the retention interval. Based on similar comparisons, the Water group also showed virtually no effects of the retention interval.
There are several possible interpretations of the maintenance of drinking in the Ethanol group across the 27-day retention interval. One possibility is based on an alcohol deprivation effect (ADE) (Sinclair and Senter, 1968; Agabio et al., 2000
; Samson and Chappell, 2001
; for review, see Li, 2000
). The ADE is well-documented as an increase in ethanol drinking following a period of abstinence; however, the ADE interpretation does not provide an account of the maintenance of CS-directed drinking observed in the Water group. These subjects were never shifted from alcohol drinking to alcohol abstinence during the retention interval, yet these rats behaved in exactly the same manner as the Ethanol group during the pre- and post-retention intervals.
An alternative view is that autoshaping of sipper CS-directed drinking is durable and well-retained. This view is consistent with the autoshaping analysis, because Pavlovian investigators have extensively documented that Pavlovian CRs are retained across long retention intervals with little or no degradation of CR performance (Mackintosh, 1974). Long-term retention of autoshaping CR performance has been reported in Pavlovian feature learning in pigeons (Nakajima, 1997
), and food-getting autoshaping in carp (Aoki, 1985
), as well as in other Pavlovian conditioning procedures (Coulter et al., 1976
; Marcant et al., 1985
; Schreurs, 1993
; Solomon et al., 1995
; Rosas and Alonso, 1997
; Solomon et al., 1998
).
In the present study, for both groups, rate of drinking was negatively related to CS duration, and this relationship between CR performance and CS duration has been widely reported by Pavlovian investigators (for reviews, see Mackintosh, 1974; Killeen, 1984
) employing a wide range of procedures, including fear conditioning (Odling-Smee, 1975
; Burkhardt and Ayres, 1979
; Ishii, 1991
; Rosas and Alonso, 1997
), conditioned enhancement and positive conditioned suppression (Meltzer, 1986
), conditioned odour aversion in rats (Rudy and Cheatle, 1978
), and conditioning of heart rate and body temperature with morphine (Schwarz-Stevens and Cunningham, 1994
). In addition, the negative relationship between CR performance and CS duration (for reviews, see Gibbon and Balsam, 1981
; Jenkins et al., 1981
; Killeen, 1984
) has also been reported by numerous autoshaping investigators employing pigeons (Balsam et al., 1978
; Gibbon and Balsam, 1981
; Balsam and Gibbon, 1982
; Balsam, 1984
; Hemmes and Brown, 1990
) and rats (Locurto et al., 1981
; Kirkpatrick and Church, 2000
).
These procedures reveal induction of drinking by Pavlovian autoshaping procedures that employ food US. It is notable that several other models of ethanol drinking in rats also arrange for the drinking of ethanol to be accompanied by the presence of food. For example, prandial drinking models of ethanol drinking provide for ethanol availability following the eating of large amounts of food (Meisch and Thompson, 1974; Neill et al., 1994
; Cunningham and Niehus, 1997
) and schedule-induced polydipsia (SIP) models of ethanol drinking provide for intermittent schedules of food presentations in a situation where ethanol is also available (Falk et al., 1972
; Hymowitz and Freed, 1974
; Colotla and Keehn, 1975
; McMillan et al., 1976
; Riley et al., 1979
).
It is appropriate to ask, therefore, if the drinking observed here may be due to either post-ingestive prandial drinking or schedule induction effects. While it is possible that either or both of these factors contributed to drinking in this study, it is unlikely that they account for a substantial portion of it. This is because all of the drinking in these Pavlovian autoshaping procedures occurs only in the brief intervals of time just prior to the ingestion of food, whereas the vast majority of drinking induced by prandial drinking or SIP procedures occurs during the post-ingestive intervals after the food has been consumed. It should also be noted that the effects of eating on drinking are estimated by pseudoconditioning controls that receive sipper CS and food US, but randomly with respect to one another. Tomie et al. (2002a,b)
provided data from two studies showing that when the sipper CS contains 6% ethanol but the sipper CS is presented randomly with respect to the food US, there is reliably less drinking than when the sipper CS and the food US are paired in the autoshaping procedure experienced by the Ethanol group in the present study.
It is appropriate to justify the use of food-deprived rats in these studies. First, it should be noted that their use is typical of traditional autoshaping studies employing food as the US (Tomie et al., 1989). Presumably, this is to ensure that the rat is hungry enough to eat the food US and experience the CSUS pairing. For this reason, it seems appropriate to initiate the testing of the autoshaping model of ethanol drinking by using the food deprivation procedures typically employed in autoshaping studies. With regard to the issue of the appropriateness of employing food deprivation in studies of ethanol drinking, it is important to note that the autoshaping model of ethanol drinking is a Pavlovian conditioning model, rather than an operant or instrumental model of ethanol self-administration. The autoshaping model is intended to evaluate the effects of non-contingent pairings of ethanol sipper and food on ethanol drinking. The drinking induced by the autoshaping technique, therefore, is due solely to the experience of ethanol sipper than food, and does not necessarily reflect on the positively reinforcing effects of ethanol. The present studies were not designed to effectively isolate ethanols positively reinforcing effect, or to provide information as to the environmental conditions most conducive to the expression of the positively reinforcing effects of ethanol (Samson et al., 2000
). While the assessment and analysis of the positively reinforcing effects of ethanol is an extremely important and complex issue, it remains orthogonal to the purpose of this study, which was to characterize the effects on ethanol drinking of experiencing the ethanol sipper just before eating.
These Pavlovian autoshaping procedures induced relatively high volumes of consumption of unsweetened 6% ethanol solutions in very brief periods of time, and therefore these procedures may provide an animal learning model of binge drinking. The rapid drinking of large volumes of ethanol, characteristic of binge drinking in humans, is observed in this study where the rats in the Ethanol group consumed 4.19 g/kg ethanol per day, even though the sipper CS was available for only a total of 500 s (8 min and 20 s) per day.
These autoshaping procedures induce binge-like drinking and do so merely by providing for repeated pairings of the ethanol sipper with food reward. The obvious suggestion is that pairings of the ethanol sipper with other types of rewards may also induce high levels of ethanol drinking. In humans, the ethanol sipper is likely to be differentially paired not only with the eating of favourite foods, but also with other rewarding and preferred activities, including social interactions, entertainment, or romance. It is likely beyond coincidence that, in humans, such circumstances appear to be highly conducive to the induction of binge-like episodes of excessive and uncontrollable ethanol intake. The intriguing possibility is that binge-like episodes of ethanol drinking are mediated by the performance of sipper CS-directed Pavlovian autoshaping CRs, and this hypothesis is supported by data, such as those presented here, showing that binge-like drinking co-varies with autoshaping CR performance (Tomie, 1995, 1996
, 2001
).
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ACKNOWLEDGEMENTS |
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FOOTNOTES |
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