Effects of swim stress on neophobia and reconditioning using a conditioned taste aversion procedure.
Abstract: Previous research has found that swim stress during a classical conditioning trial attenuates conditioned taste aversion (CTA). In the current study, rats were used to examine the effects of inescapable swim stress on the habituation of neophobia to a flavored solution and reacquisition of an extinguished conditioned taste aversion. In Experiment 1, subjects were initially exposed to a taste, with some subjects receiving a swim experience to assess the level of neophobia on a subsequent taste-exposure test. Rats in Experiment 2 were given a taste-LiCI trial followed by extensive CS-alone extinction trials. Subjects then received the tast-LiCI pairing again, followed for some by a swim experience to examine its effect on subsequent reconditioning. Swim stress influenced CS processing on the final extinction trial. Thus, reacquisition was attenuated by swim, but there was no effect of swim stress on the attenuation of neophobia. These results are discussed in terms of the effects of stress on CS processing.

Key words: taste aversion, neophobia, reacquisition, swim stress, classical conditioning, extinction
Article Type: Report
Subject: Phobias (Physiological aspects)
Stress (Psychology) (Physiological aspects)
Psychophysiology (Research)
Authors: Walker, Jennifer M.
Ramsey, Ashley K.
Fowler, Stephanie W.
Schachtman, Todd R.
Pub Date: 03/22/2012
Publication: Name: The Psychological Record Publisher: The Psychological Record Audience: Academic Format: Magazine/Journal Subject: Psychology and mental health Copyright: COPYRIGHT 2012 The Psychological Record ISSN: 0033-2933
Issue: Date: Spring, 2012 Source Volume: 62 Source Issue: 2
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 288689701
Full Text: Stress during learning can influence the processing of information and subsequent performance (e.g., Payne, Nadel, Britton, & Jacobs, 2004). Bourne, Calton, Gustayson, and Schachtman (1992) and Revusky and Reilly (1989), using inescapable swim as a source of stress, examined the effects of this stressor on conditioned taste aversion (CTA) in rats. CTA refers to learning to avoid consumption of a taste solution after that solution has been paired with a consequence that produces internal malaise (e.g., MG).

Bourne et al. (1992) and Revusky and Reilly (1989) suggested that a swim stress experience reduces the effectiveness of the unconditioned stimulus (US; e.g., the drug that produces internal malaise, such as TACO on the conditioning trial. However, in contrast to stress affecting the effectiveness of the US, swim stress may attenuate the acquisition of its association with the CS (conditioned stimulus), either by impacting the processing of the CS or influencing the associative link between the CS and the US. Processing refers to a change in behavior that results from the presumed activation of representations of events in memory and the activities involving the association of such events. The role of swim stress on CS processing has not been given much attention (cf. Smith, Fieser, Jones, & Schachtman, 2008). Swim stress may serve as a distracting event that reduces the amount of attention allocated to the CS (e.g., for effects using a second taste CS, see Green & Parker, 1975, and Robertson & Garrud, 1983; see also Wagner, Rudy, & Whitlow, 1973), thereby hindering the conditioning that might otherwise occur on that conditioning trial to a target CS.

In order to examine the effects of swim stress on CS processing, Smith, Fieser, Jones, and Schachtman (2008) examined the effects of swim stress on latent inhibition. Latent inhibition refers to the poor learning that occurs for a CS if nonreinforced exposures to the CS are administered prior to CS-US pairings (e.g., Lubow & Moore, 1959). Smith et al. gave rats a 5-min period of swim stress following each of three CS preexposures (saccharin-alone exposures). Then the rats were given saccharin-LiC1 pairings to examine the effects of the CS preexposures on conditioning. Control conditions did not receive any preexposure to saccharin. On single-bottle test trials with saccharin, the control conditions, as expected, showed a substantial aversion to the flavor. The group given saccharin preexposure without any swim stress exhibited a typical latent inhibition effect in which the conditioned response (CR) was relatively poor. The group given swim stress during the preexposure phase showed substantial conditioning, such that the swim experience attenuated the latent inhibition effect. The effect of swim stress administered during CS preexposure on later conditioning argues against the swim stress influencing the perceived aversiveness of the US (i.e., effects of LiC1) or impacting the CS-US association; it suggests that swim stress can influence CS processing.

The present study examined the effects of inescapable swim on two additional conditioning phenomena in which CS-alone trials occur (i.e., phenomena that presumably concern processing of the CS): the habituation of neophobia and the extinction of associations (specifically, the effects of swim on the reacquisition of extinguished associations). The experiments examined whether a single swim-stress experience would influence processing of a taste CS during trials in which a US (e.g., LiC1) is absent--as Smith et al. (2008) found using swim stress and a latent inhibition procedure. One swim-stress experience was used since previous research (Bourne et al., 1992; Revusky & Reilly, 1989) has found that a single swim-stress episode can impact CTA.

Experiment 1

Neophobia to a flavor is defined as an increase in taste consumption from the initial presentation of the taste to the second exposure to that taste (Domjan, 1977). Stress at the time of initial flavor exposure may influence how well the stimulus is processed and thereby impact (e.g., potentially reduce) the degree to which the taste is deemed familiar and reduce consumption (maintain greater neophobia) during the second (test) exposure. Many researchers have used the presentation of a second "distracting taste" to examine its influence on the habituation of neophobia to a flavored target solution (e.g., Green & Parker, 1975; Robertson & Garrud, 1983). Experiment 1 sought to examine the effects of swim stress on the habituation of neophobia to a taste CS. In order to maximize sensitivity to observing an effect of swim stress on flavor processing, a variety of flavors and administration procedures were used across the different experiments conducted.

Method

Subjects and apparatus. Experimentally na ve, adult Sprague-Dawley-derived male and female rats from the University of Missouri breeding colony were individually housed in hanging, stainless-steel wire mesh cages that measured 24 x 17.8 x 18.2 cm (1 x w x h) with ad lib access to lab chow (Purina, St. Louis, Missouri). Subjects were gradually water deprived over the course of 6 days prior to the start of the experiment, culminating in 10-min water access each day. The rats of Experiment 1 (Experiments 1A-1C) had a body-weight range of 188-510 g, and the groups were counterbalanced for mean body weights. The large weight range was a result of the fact that rats of different ages were used in each experiment and the sex of the rats varied in certain experiments. Water access occurred in the home cage after each day's experimental manipulations, approximately 23 hr prior to the experimental session of the following day. Subjects were maintained on a 16-hr light/8-hr dark cycle, and treatments occurred during the middle of the light portion of the cycle. The rats were handled two to three times prior to the experimental manipulations. All treatments (other than administration of the swim stress) occurred in the home cage. Swim stress exposure occurred in a 121.1-liter cylindrical plastic container measuring 57.2 cm (diameter at base) x 82.6 cm (height) that was approximately 75% full of room-temperature water. A 50-ml plastic drinking tube with a rubber stopper was used to administer flavored solutions (except where noted). On each day of all experiments reported here, all subjects received 10 min of access to water in glass drinking bottles in the home cage to ensure replenishment of fluid. This work was carried out in accordance with the University of Missouri Animal Care and Use Committee (Protocol 1159).

The experiments used either 0.2% (w/v) sodium saccharin (Sac, Sigma Co., St. Louis, MO), 5% (v/v) vinegar (Vin, Heinz, Pittsburgh, PA), or 6% (v/v) banana-flavored (McCormick Inc., North Lauderdale, FL) solutions. These flavors and concentrations were selected based on pilot data (see the "Procedure" section) and earlier published work from our laboratory using vinegar and saccharin concentrations (e.g., Calton, Mitchell, & Schachtman, 1996; Kasprow & Schachtman, 1993). All solutions described in all experiments contained fresh tap water. Different levels of neophobia may be differentially sensitive to the effects of swim stress. Therefore, different flavored solutions were used in Experiment 1 to attempt to maximize sensitivity to observing an effect of swim on the attenuation of neophobia.

Procedure. The designs of Experiments 1A-1C are shown in Table 1. Prior to Day 1 of Experiment 1A, 16 male and female rats were divided into two groups: stress (n = 8) and no stress (n = 8), which were counterbalanced for body weight (as mentioned previously) as well as sex. The stress group was given 10 min of free access to the 0.2% saccharin solution in the drinking tubes and then immediately placed into the container of water for 5 min, after which they were towel dried and returned to the home cage. This particular swim-stress procedure was used because earlier work has found it to be effective in influencing CTA conditioning (Bourne et al., 1992; Revusky & Reilly, 1989). The experiment used a stronger concentration of saccharin (0.2%) than the concentration that is frequently used for conditioning and reconditioning experiments (e.g., Experiment 2 of the current study; see also Hart, Bourne, & Schachtman, 1995) in order to produce a neophobia response. The nostress group was given 10 min of free access to 0.2% saccharin without the swim experience. On Days 2 and 3, all rats were given free access to saccharin for 10 min to assess the extent of habituation of neophobia (an increase in consumption on Days 2 and 3 relative to Day 1).

In Experiment 1B, 30 male and female rats were divided into four groups (counter-balanced for sex and body weight): no stress (n = 7), stress before (n = 8), stress after (n = 8), and control (n = 7). Rats in Experiment 1A, as discussed in the following section, consumed a considerable amount of solution across all days of the study. This may have contributed to rapid habituation of neophobia during this single bout of exposure. Therefore, Experiment 18 sought to limit the amount of consumption on Day 1 by infusing the solution directly into the animals' mouths to control the amount consumed. The oral-infusion procedure also insured comparable exposure to the taste for different swim conditions. Banana-flavored solution was also used to produce stronger neophobic effects that might result in group differences on Day 1 due to the swim experience. Pilot data in our laboratory found pronounced neophobia using this concentration of banana-flavored solution; that is, rats consumed significantly more on Day 2 relative to Day 1, F(1, 5) = 9.57, p < .03.

On three preliminary days of Experiment 1B, the rats were given an oral infusion of 2 ml of water to acclimate them to the oral-infusion procedure. On Day 1, the rats in the no-stress group were orally infused with 2 ml of 6% banana-flavored solution, while the control group was orally infused with water. The rats in the stress-before group were given swim stress for 5 min, followed immediately by oral infusion of 2 ml of banana-flavored solution. The stress-after group was given a 2-ml oral infusion of the banana-flavored solution and then immediately given swim stress for 5 min. On Days 2 and 3, all rats were given 10 min of free access to the banana-flavored solution in the drinking tubes.

Experiment 1C was procedurally identical to Experiment 1B, except that 24 male and female rats were used, and the flavor used was 5% vinegar. The groups were identical to those used in Experiment 1B: no stress, stress before, stress after, and control (ns = 6). The criterion for rejection of the null hypothesis was p = .05 for all experiments.

Results and Discussion

On Day 1 of Experiment 1A, the no-stress group consumed (mean [+ or -] SEM) 14.0 ([+ or -] 2.4) ml, while the stress group consumed 14.2 ([+ or -] 1.4) ml. On the two test trials (Days 2 and 3), the no-stress group consumed 17.9 ([+ or -] 2.1) and 19.7 ([+ or -] 1.6) ml, respectively, while the stress group consumed 18.2 ([+ or -] 0.9) and 21.0 ([+ or -] 1.1) ml on these trials. The rats did increase their consumption from Day 1 (initial exposure) to Day 2 (Test Day 1), indicating that a significant attenuation of neophobia occurred for both groups. This effect was confirmed by an analysis of variance (ANOVA), which found a main effect of day, F(1, 14) = 8.90, p < .01, but neither a main effect of group nor an interaction, Fs < 1. An ANOVA conducted on the test scores (Days 2 and 3) yielded no main effect of group (F < 1), a marginally significant effect of day, F(1, 14) = 4.19, p = .06, and no interaction, F < 1.

The test results from Experiments 1B and 1C are shown in Figures 1 and 2, respectively. An ANOVA conducted on the test data from Experiment 1B obtained no significant main effect of group, F(3, 26) = 2.26, p > .10. Subjects increased their flavor consumption across test trials (i.e., a main effect of day occurred), F(1, 26) = 9.68, p < .005, and there was no interaction of group and day, F(3, 26) = 1.20, p > .30. An ANOVA conducted on the test data for Experiment 1C obtained no main effect of group, F < 1, and no group-by-day interaction, F < 1, and the subjects did increase their consumption across the two test days as revealed by a main effect of day, F(1, 20) = 26.17, p < .01. Swim stress did not influence the attenuation of neophobia using the present procedures and conditioned stimuli. Only a single swim stress was given in these experiments, consistent with the procedure used by Bourne et al. (1992) and Revusky and Reilly (1989). The swim stress may have been more impactful had it been given after several exposures to the flavored solution; however, the attenuation of neophobia occurs largely between the first and second exposures to a flavor, making several swim exposures an insensitive procedure for producing an effect.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Experiment 2

Experiment 2 examined the effects of swim stress on another phenomenon involving CS-alone presentations: the reacquisition of an extinguished taste aversion. Swim stress was administered during the final extinction trial prior to a subsequent phase in which the CS was once again paired with the US (i.e., reconditioning). Extinction refers to the presentation of CS-alone exposures following CS-US pairings, which results in a loss of the CR originally acquired during conditioning. Some learning theorists have stated that CS-alone extinction results in a decrease in attention or associability (Pearce & Hall, 1980). If a CS is given extensive CS-alone extinction presentations following CS-US pairings, and the CS is then repaired with the US, reconditioning will be slow (e.g., Bouton, 1986; Bouton & Swartzentruber, 1989; Danguir & Nicolaidis, 1977). This slow reacquisition may be due to a low level of attention or associability to the CS as a result of the extinction trials. Post-CS surprising events have been shown to augment attention to a CS and improve conditioning on subsequent trials (e.g., Hall & Pearce, 1982). Swim stress, as a surprising postflavor event, administered on an extinction trial prior to reconditioning may promote attention to the CS and facilitate reacquisition. Experiment 2 examined if swim stress administered on the final extinction trial might enhance attention to an extinguished CS and thus produce greater associability of the cue on a subsequent reconditioning trial. Such an effect would show that swim can influence CS processing. Moreover, similar to the effect produced by Smith et al. (2008)--and in contrast to the effects by Revusky and Reilly (1989) and Bourne et al. (1992), in which swim reduced CTA--such an effect would demonstrate that swim stress can enhance conditioned responding on subsequent test trials.

Method

Subjects and apparatus. Experiment 2 used 22 male na ve rats purchased from a commercial breeder (Sasco, Lincoln, NE) that ranged in body weight from 160-250 g. Lid (Sigma, St. Louis, MO) was administered using a 25-ga, 1.59-cm hypodermic needle. All other details of the subjects and the apparatus were identical to those of Experiment 1 except where noted in the following section.

Procedure. The design of Experiment 2 can be seen in Table 2. Day 1 (Phase 1) of Experiment 2 involved a 10-min exposure to either a 0.1% saccharin solution (Groups R and R-Stress, in which R refers to reacquisition of an aversion to saccharin) or a 1.5% coffee solution (Groups C and C-Stress, in which C refers to control, such that these subjects did not receive initial training with saccharin) followed immediately by 0.3 M Cl at 1.33% body weight. Previous research on reacquisition effects with a CTA procedure has used saccharin as the conditioned stimulus and has typically used a concentration of 0.1%; therefore, this concentration was used in the present study. The different treatments were also counterbalanced for sex and body weight. On Day 2, no treatments occurred to allow the rats to recover from illness, with the exception of the rats' daily water exposure. Phase 2 occurred on Days 3-11. On Days 3-10 each animal received a 10-min exposure to the solution it had received on Day 1 but without LiC1 (i.e., extinction). Following treatment on Day 10, the subjects that had been conditioned and extinguished with saccharin were assigned to Groups R (n = 6) and R-Stress (n = 6); those that had received coffee were assigned to Groups C (n = 5) and C-Stress (n = 5), while counterbalancing for body weight and consumption of the flavored solution prior to Day 11. On Day 11 (the final extinction trial), the rats in Groups R-Stress and C-Stress received an extinction trial exactly like those on Days 3-10, except that immediately afterward they received a 5-min placement in the water-filled container as a swim experience. Groups R and C remained in their home cage after the taste exposure. On Day 12 (Phase 3), all subjects received saccharin for 10 min followed by an injection of 0.15 M Lid! at 1% body weight. A lower dose was used to prevent floor effects for consumption on the test trials. We used a single reconditioning trial (for saccharin-trained rats) prior to testing because earlier work found that this produced a reacquisition effect that was modest and might be more sensitive to producing differences between stressed and non-stressed conditions (i.e., earlier work obtaining slow reacquisition effects in taste aversion has used two such conditioning trials; Calton et al., 1996; Hart et al., 1995). On Day 13, the animals were given no treatments except for their daily exposure to water. All subjects were given a 10-min exposure to saccharin during testing on Day 14. This procedure was used because a highly similar procedure has been found to produce slow reacquisition of CTA in earlier studies (e.g., Hart et al., 1995).

Results and Discussion

In Experiment 2, Groups R-Stress, R, C-Stress, and C consumed (mean [+ or -] SEM) 8.8 ([+ or -] 1.2), 8.5 ([+ or -] 0.9), 5.5 ([+ or -] 1.6), and 4.6 ([+ or -] 0.7) ml, respectively, on the conditioning trial. Consumption was higher for the saccharin solution than the coffee solution on Day 1 given that saccharin was apparently more palatable for the subjects, F(1, 18) = 9.05,p < .01, and the groups showed a decrease from Day 1 to Day 3, F(1, 18) = 131.62. Groups R-Stress, R, C-Stress, and C consumed 1.0 ([+ or -] 0.2), 0.9 ([+ or -] 0.3), 0.9 ([+ or -] 0.3), and 0.8 ([+ or -] 0.1) ml, respectively, on the first extinction trial. These same groups consumed 8.3 ([+ or -] 1.6), 9.7 ([+ or -] 1.9), 8.3 ([+ or -] 1.9), and 6.1 ([+ or -] 1.8) ml, respectively, on the final extinction trial. The groups increased their consumption during extinction, F(1, 18) = 20.53, but, importantly, no group effect or interaction occurred, Fs < 1.05.

Saccharin consumption on Days 12 and 14 of Experiment 2 is represented in Figure 3. An ANOVA conducted on the Day 12 data found no main effect of flavor, F(1, 18) = 4.04, p > .05. Group R-Stress did produce a slightly greater consumption of saccharin numerically on Day 12, but it did not differ from the other groups. A poorer aversion occurred on Day 14 as a result of the Day 12 reconditioning trial for Groups R and R-Stress relative to Groups C and C-Stress, F(1, 19) = 12.74, p < .005. This effect reflects the slow reacquisition effect in a CTA procedure, as obtained in earlier reports (e.g., Calton et al., 1996; Danguir & Nicolaidis, 1977; Hart et al., 1995). Specific comparisons found that Group R-Stress showed a significantly poorer aversion on Day 14 than both of the two coffee control conditions, Fs > 12.10, ps < .01, while Group R did not show a greater aversion on Day 14 compared to these control conditions, ps > .10. These comparisons reveal that Group R-Stress exhibited evidence of slow reacquisition on Day 14, while Group R did not. However, the poorer aversion by Group R-Stress relative to Group R was only marginally significant, F(1, 10) = 3.31, .05 < p < .10.

[FIGURE 3 OMITTED]

General Discussion

Revusky and Reilly (1989) and Bourne et al. (1992) showed that swim stress attenuates CTA when it is administered near the time of the flavor LiC1 pairings. These authors suggested that swim stress impacts the effectiveness of the US on the conditioning trial. The present experiments examined whether swim stress impacts CS processing by administering swim stress during treatments in which the CS is presented in the absence of the US. Swim stress did not exert an influence on the attenuation of neophobia. Smith et al. (2008) found that swim stress administered at the time of CS preexposures during a latent inhibition procedure attenuated latent inhibition, presumably by reducing CS processing. If a similar effect had occurred during the flavor exposures in the present neophobia experiments, then, again, it would be expected that neophobia would be maintained on the test trials (low consumption was predicted). No such effect occurred in the present Experiment 1, despite the use of several parameters and procedures. Following a flavor presentation with swim stress does not appear to produce a distracting effect on processing of the flavor. If swim served as a distracting event (reducing the degree to which the flavor is processed), then habituation of neophobia to the flavor would be reduced (neophobia would be maintained). Many researchers (e.g., Green & Parker, 1975; Robertson & Garrud, 1983) have used a postflavor event (such as a second, surprising flavor) to reduce the habituation of neophobia. Thus, posttrial events can serve such a function. It should also be noted that the latent inhibition study by Smith et al. used three CS preexposures, with swim stress occurring each time these exposures occurred, and enhanced conditioning resulted. Therefore it is possible that multiple instances of CS exposure and swim are needed to produce such an effect on neophobia.

The representation of a taste without an aversive consequence may produce a "safe taste memory" (e.g., Bermudez-Rattoni, 2004). The cholinergic system appears to be involved in the creation of safe memories, as demonstrated by research showing that scopolamine, a muscarinic ACh receptor antagonist, injected at the time of the initial presentation of the taste will lower consumption when the flavor is subsequently presented (producing maintenance of the neophobia response; Gutierrez, Tellez, & Bermudez-Rattoni, 2003). The results of the present study are not consistent with any influence on the cholinergic system, at least to the extent that changes in the cholinergic system could be produced by swim stress and that such changes can affect the attenuation of neophobia. However, it is known that swim stress can change ACh levels in the nucleus accumbens (Rada, Colasante, Skirzewski, Hernandez, & Hoebel, 2006).

Nakajima and Masaki (e.g., Nakajima & Masaki, 2004) have found that swim can serve as a US and produce CTA to a flavor. In the current study, no aversion to the flavor was found in the groups given stress in Experiment 1, although such an aversion might have formed if several flavor swim pairings had occurred. There are many differences between the procedure used by Nakajima and his colleagues, which obtained CTA produced by swim, and the present procedure, which found no such effect. Nakajima's laboratory typically used a swim exposure of 15-30 min (in contrast to the present 5-min period) as well as a two-bottle choice test (in contrast to the present single-bottle test; cf. Nakajima & Masaki, 2004, in which a short swim interval and a single-bottle test were used).

Swim stress did have an effect on the reacquisition of an aversion to a previously extinguished flavor to the extent that the group given swim showed evidence of slow reacquisition relative to the control condition, while the no-stress group did not. That is, Experiment 2 found an effect in which swim experienced on the final extinction trial slowed the rate of subsequent conditioning. Similar to the findings of Smith et al. (2008) using a latent inhibition procedure, the present results show that swim stress can influence processing of the stimulus on trials in which a conditioned stimulus occurs but an unconditioned stimulus is not present.

The results of Experiment 2 provide no evidence that swim can increase attention or associability to an extinguished CS. An increase in attention or associability produced by swim stress administered on the final extinction would be expected to cause the flavor to condition more readily on the subsequent conditioning trial. Instead, poorer conditioning occurred for the group administered swim stress prior to the reconditioning trial.

It is possible that swim stress did disrupt processing of the ninth and final extinction trial through a distraction mechanism (such that the effects of this extinction trial were negated). However, one fewer extinction trial for Group R-Stress would be expected to produce, if anything, better reacquisition, and yet Group R-Stress showed less of an aversion. In sum, swim stress did not enhance attention/associability of the flavor, nor did it serve as a distracting event that disrupts processing. We did not, of course, provide a direct measure of whether the distracting event influenced processing of the target CS. However, earlier work has also claimed that posttrial distracting events influence processing of the target in short-term memory (Robertson & Garrud, 1983; Wagner, 1976), but it remains an assumption that posttrial swim impacted CS processing in Experiment 2 of the current study by slowing additional conditioning. Although it was expected that swim would facilitate reacquisition rather than slow conditioning, it is interesting that Robertson and Garrud, in their work using flavor CSs, stated, "It was found that a distractor need not always disrupt habituation to a test stimulus. Instead, the opposite effect may be obtained, vis., habituation to a test stimulus may be enhanced by representation of a distractor. Whether a distractor disrupts or enhances habituation to a test stimulus appears to depend on the stimulus characteristics of the distractor and the test stimulus" (1983, p. 474). If we had used different flavors for the present Experiment 2, an enhancement of conditioning produced by the distractor may have been obtained. Also, since we used inescapable swim stress in the present experiments, it is not known if escapable swim stress would have impacted behavior. It is known that controllable and uncontrollable stress have different physiological mechanisms (e.g., Whitehouse, Blustein, Walker, Bersh, & Margules, 1985). It is also not clear if handling cues added to the stress provided by the swim experience.

The poorer aversion in the results of Experiment 2 by subjects that received swim stress does not support the claim that swim promoted a taste aversion (i.e., swim serving as an unconditioned stimulus) for rats given swim on the final extinction trial, although swim can, as mentioned, promote CTA in some situations (Masaki & Nakajima, 2006; Nakajima & Masaki, 2004).

As noted, Rada et al. (2006) found that acetylcholine levels changed as a function of swim stress; an increase in levels was seen 24 hours after the swim experience, thereby showing that swim stress during extinction can cause neural changes that could impact a (re)conditioning trial 24 hours later.

The existing literature examining the effects of swim stress on learning has produced a myriad of findings, such that swim stress sometimes promotes conditioning (e.g., Masaki & Nakajima, 2006) and sometimes attenuates conditioning (Bourne et al., 1992; Revusky & Reilly, 1989); swim can also attenuate learning during CS-alone trials to facilitate learning during subsequent CS US pairings (Smith et al., 2008). The finding that swim at the time of an extinction trial can produce poor subsequent conditioning reveals that swim can influence CS processing and, in contrast to the results of Smith et al., does not always facilitate subsequent conditioning (i.e., the reversal of the latent inhibition effect) but can also attenuate it. This reduction in conditioning parallels the poor conditioning obtained by Bourne et al. (1992) and Revusky and Reilly (1989). Yet, the latter effects stemmed from a procedure in which swim stress occurred at the time of the conditioning trial, whereas the present slow reacquisition effect involved swim during CS-alone exposure prior to conditioning. Clearly swim stress can exert numerous effects on CTA, and the present results extend these findings by examining the effects of swim stress using procedures in which swim occurs during CS-alone trials (habituation of neophobia and the final extinction trial before reconditioning).

There are many reports of manipulations that occur at the time of CS US pairings or CS presentations during training that influence performance to the stimulus (e.g., impact habituation of neophobia) differently from their effects on conditioning. That is, a treatment can influence responding to a CS on the conditioning trial without influencing the conditioning process itself. Treatments can also influence conditioning without impacting performance to the CS on the conditioning trial. For instance, presentation of a second CS (a distractor) during initial presentation of the target CS in a habituation-of-neophobia procedure may have no effect on such habituation if a long interval (24 hours) occurs between such training and the final habituation test (Kaye, Gambini, & Mackintosh, 1988); however, such a treatment can greatly influence conditioning to the CS (e.g., Lubow, 1989). Kaye et al. also found that habituation and conditioning can be dissociated based on temporal placement of the distractor relative to the target CS during initial exposure to the events (see also Mackintosh, 1987). Moreover, some models of classical conditioning (Pearce & Hall, 1980) have posited that one CS variable (alpha) reflects the "associability of a CS," which impacts the rate of conditioning, while another variable reflects a performance variable. Therefore, mechanisms underlying postswim performance should be further dissociated from those involving the effects of swim on conditioning.

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Jennifer M. Walker, Ashley K. Ramsey, Stephanie W. Fowler, and Todd R. Schachtman

University of Missouri

Correspondence concerning this article should be addressed to Todd R. Schachtman, Department of Psychological Sciences, 210 McAlester Hall, University of Missouri, Columbia, MO 65211. E-mail: SchachtmanT@missouri.edu
Table 1

Design of Experiment 1

               Experiment 1A

Group          Exposure (Day 1)       Test (Days 2-3)

Stress         Saccharin swim         Saccharin alone
No stress      Saccharin alone        Saccharin alone

               Experiments 1B and 1C

Group          Exposure (Day 1)       Test (Days 2-3)
No stress      Flavor alone           Flavor alone
Stress before  Swim-flavor            Flavor alone
Stress after   Flavor-swim            Flavor alone
Control        Water alone            Flavor alone

Note. Experiment 1A: Saccharin=0.2% (w/v) saccharin with free access to
saccharin in drinking tubes for all exposures; swim=5 min of inescapable
swim. Experiment 1B; Flavor was a 0.2% (v/v) banana-flavored solution,
of which 2 ml were infused on Day 1 and to which free access occurred on
Days 2-3; swim=5 min of inescapable swim. Experiment 1C: Flavor was a 5%
(v/v) vinegar solution, of which 2 ml were infused on Day 1 and to which
free access occurred on Days 2-3; swim=5 min of inescapable swim.


Table 2

Design of Experiment 2

Group     Phase 1         Phase 2       Final Phase
          Conditioning    Extinction    2
          (Day 1)         (Days         Extinction
                          3-40)         Trial
                                        (Day 11)

R-Stress  Saccharin LiCI  Saccharin     Saccharin
                          alone         swim

R         Saccharin LiCI  Saccharin     Saccharin
                          alone         alone

C-Stress  Coffee LiCI     Coffee alone  Coffee swim

C         Coffe-LiCI      Coffee alone  Coffee alone

Group     Phase 3         Test (Day 14)
          Conditioning
          (Day2)

R-Stress  Saccharin LiCI  Saccharin
                          alone

R         Saccharin LiCI  Saccharin
                          alone

C-Stress  Saccharin LiCI  Saccharin
                          alone

C         Saccharin-LiCI  Saccharin
                          alone

Note. Saccharin=0.1% (w/v) saccharin with free access to saccharin in
drinking tubes for all exposures; LiCI=0.3 M at 1.33% body weight in
Phase 1 and 0.15M at 1% body weight in Phase 3; swim=5min of inescapable
swim; coffee=1.5% decaffeinated coffee. All solutions were administered
with free access for 10 min. No treatments occurred on Day 13.
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