- Email: [email protected]
Distractor effects upon habituation of complex stimuli
Behavioural Processes 90 (2012) 204–209
Contents lists available at SciVerse ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Distractor effects upon habituation of complex stimuli夽 Antonio A. Artigas a,b,∗∗ , Joan Sansa a,b , Jose Prados c,∗ a
Departament de Psicologia Bàsica, Universitat de Barcelona, Spain Institut de Recerca en Cervell, Conducta i Cognicio, IR3C Barcelona, Spain c School of Psychology, University of Leicester, University Road, LE1 9HN Leicester, United Kingdom b
a r t i c l e
i n f o
Article history: Received 12 July 2011 Received in revised form 16 December 2011 Accepted 26 January 2012 Keywords: Distractor effects Generalization decrement Wagner’s SOP theory
a b s t r a c t In two experiments, rats were given serial forward (the target followed by the distractor) or backward (the distractor followed by the target) exposure to two compound flavor stimuli that could be either similar (Salt–X/AX) or dissimilar (Salt–X/AY, Experiment 1; Salt/AX, Experiment 2). Following pre-exposure, the Salt element was presented in a compound with a novel flavor, N. The salience or effectiveness of the Salt element was then assessed by presenting the new flavor, N, under a state of salt appetite. Experiments 1 and 2 revealed that the order of presentation modulated the habituation of the Salt element only when the distractor was similar to the target: the Salt element was more salient after forward than backward pre-exposure. In the groups Dissimilar the order of pre-exposure was irrelevant; however, when the Salt element was presented in compound with a second element (Salt–X, Experiment 1), its salience was preserved, whereas when it was presented alone (Salt, Experiment 2) its salience was significantly reduced. These results, which are discussed in terms of Wagner (1981) theory of habituation, inform about the way in which stimuli presented closely in time are processed. © 2012 Elsevier B.V. All rights reserved.
1. Distractor effects upon habituation of complex stimuli Non-reinforced exposure to stimuli has been shown to affect the way in which they can control an animal’s behavior. For example, repeated presentations of a stimulus result in a loss of its salience or perceptual effectiveness, declining the strength of any responses it initially elicited—a process of habituation (e.g., Rankin et al., 2009; Thompson and Spencer, 1966). Such habituation, however, can be disrupted by the presentation of an additional stimulus or distractor closely in time (e.g., Green and Parker, 1975; Shanks et al., 1986; Thompson and Spencer, 1966). Several factors have been found to modulate the distractor effect: the similarity between the target and the distractor (e.g., Robertson and Garrud, 1983; Kaye et al., 1988); and the order of presentation of the target and the distractor (e.g., Robertson and Garrud, 1983). In the study by Robertson and Garrud (1983), rats were given one exposure trial to a particular flavor and the habituation of its neophobia—the natural response of rats to new flavor stimuli—was then assessed. Disruption of habituation was observed when the
夽 This work was supported by a grant from the Spanish Ministerio de Ciencia e Innovación (Ref: SEJ2007-67416) to the authors. ∗ Corresponding author at: School of Psychology, University of Leicester, Lancaster Road, LE1 9HN Leicester, United Kingdom. Tel.: +44 116 2297150; fax: +44 116 2297196. ∗∗ Corresponding author at: Departament de Psicologia Bàsica, Universitat de Barcelona, Pg. de la Vall d’Hebron 171, 08035-Barcelona, Spain. E-mail addresses: [email protected] (A.A. Artigas), [email protected] (J. Prados). 0376-6357/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2012.01.009
target flavor was followed by a dissimilar stimulus (sucrose followed by coffee, a post-distractor effect), but not when the target was followed by a similar distractor (lemon followed by coffee). Interestingly, when they reversed the order in a second experiment, the pattern of results was also reversed: disruption of habituation was observed when the target was preceded by a similar stimulus (coffee preceded by lemon, a pre-distractor effect), but not when it was preceded by a dissimilar distractor (coffee preceded by sucrose). (Robertson & Garrud presented independent evidence that the similarity between coffee and lemon was higher than the similarity between coffee and sucrose.) To account for this intriguing pattern of results, Robertson and Garrud (1983) offered an explanation based on Wagner (1976, 1981) theory of stimulus processing. The theory assumes that habituation depends on how well stimuli are processed in a limitedcapacity short term memory (STM) unit, and distinguishes between two activation states in the STM. Presentation of a stimulus would result in full activation of the stimulus in the STM unit—the A1 state in which the stimulus will be fully processed. Subsequently, activation would decay into a marginal level of activation—the A2 state in which the stimulus is active but subject to limited processing (Atkinson and Shiffrin, 1968; Wagner, 1981). Interestingly, any elements already in A2 will not be provoked to the primary state of activation in A1, even if the stimulus is again physically presented. According to Robertson and Garrud (1983), this would also apply for a similar stimulus: if stimulus X is in A2, presentation a very similar stimulus, X’, would not result in its activation in A1 in the STM unit, and stimulus X’ would not be processed. However, serial
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
presentation of two distinctive stimuli (X and Y) would result in the second one displacing the first one from the capacity limited STM unit, resulting in good processing of the second but not the first event. Going back to the Robertson and Garrud (1983) experiments, when the target flavor is immediately followed by a distinctive distractor, the target would be displaced from STM and its processing would be interrupted. However, when a very similar distractor follows the presentation of the target, access to the STM unit by the distractor would be prevented, and the target would be fully processed. That would explain why a post-distractor effect can only be observed when the target and the distractor are dissimilar. On the other hand, a dissimilar target would be able to displace a predistractor from the STM unit, and full processing of the target would result in normal habituation; however, a similar pre-distractor would prevent the access of the target to the STM unit, disrupting the habituation process. This could account for the pre-distractor effect that was observed when the target and the distractor were very similar. Kaye et al. (1988) pointed out that the effect observed by Robertson & Garrud with a similar pre-distractor is a surprising outcome. Even assuming that a similar pre-distractor could prevent the access of the target to the capacity-limited processor, this should be counteracted by the generalization of the habituation acquired by the distractor to the target. Kaye et al. carried out a series of experiments which aimed to directly assess the interaction between the order of presentation and the similarity between the target and the distractor reported by Robertson and Garrud (1983). In one of the experiments reported by Kaye et al., animals were given exposure to a target lemon flavor stimulus. When lemon was preceded or followed by the presentation of a dissimilar saline solution, significant disruption of habituation to the target lemon flavor was observed. However, when the lemon flavor was preceded or followed by the presentation of a similar flavor, coffee, habituation proceeded almost normally (Kaye et al., 1988, presented independent evidence that the coffee stimulus was salient enough to disrupt habituation of other dissimilar stimuli, like a saline-sucrose mixed solution; and that coffee was more similar to lemon than the saline solution.) The results reported by Kaye et al. (1988) suggest that the similarity between the target and the distractor modulates the distractor effects; the order of presentation, however, was found to be irrelevant. The authors of the study proposed an explanation of the distractor effects based on the generalization decrement principle. Exposure (in any order) to two flavor stimuli can be said to involve exposure to their unique features (A and B, where A represents what is unique to lemon, and B what is unique to coffee, for example) as well as exposure to their common elements (X). The proportion of X common elements will vary according to the similarity of the two stimuli: we can expect the proportion of X elements to be higher when using similar flavors—lemon and coffee—than when using dissimilar flavors—lemon and sucrose. In the case in which the two stimuli are very similar, we could assume that habituation to AX will generalize to BX via X. In the case in which the target and the distractor are dissimilar, we can expect this generalization to be lower (because the low proportion of common elements). And this is the outcome that was observed in the experiments reported by Kaye et al. (1988). There is, however a limitation in the analysis carried out by Kaye et al. (1988): whatever happens in the test will depend on the habituation to the common elements, X; but differences in the habituation to the unique features of two similar stimuli (A, what is unique to lemon; and B, what is unique to coffee) would be masked by the habituation acquired by the common elements. In fact, there are reasons to believe that the order of exposure to the target and the distractor could have an effect upon the habituation
205
to the unique elements A and B. Going back to the explanation proposed by Robertson and Garrud (1983) for the distractor effects, if two similar stimuli are presented within a short period of time, the first stimulus to gain access to the STM unit would prevent the access to the processor of the other one. If the target stimulus is presented first (AX → BX), both its unique and common features (A and X) would be adequately processed, resulting in full habituation; and only the unique features of the distractor (B) would remain intact—because they get no access to the processor. However, if the target follows the distractor (BX → AX) its unique features (A) would remain intact. That being the case, a salient A element presented in compound with a habituated X element could control the performance of the individual during the test, resulting in a pre-distractor effect (as observed in the experiments by Robertson and Garrud, 1983). If two dissimilar stimuli are used (the target AX and the distractor BY), the opposite pattern of results could be expected. In the AX → BY arrangement (the target followed by the distractor), the distractor would displace the target from the capacity-limited STM unit. In that way, A and X would remain intact, resulting in a post-distractor effect. However, in the BY → AX arrangement is the target who displaces the distractor from the STM unit, ensuring full processing of its elements, A and X. This would result in habituation of all the elements of the target AX (absence of a pre-distractor effect). And this is exactly what Robertson and Garrud observed in their experiments. The experiments reported by Robertson and Garrud (1983) and Kaye et al. (1988) seem to suggest the action of two different mechanisms that modulate the habituation of the elements of the pre-exposed flavors. However, it is difficult to ascertain how these mechanisms work because in their experiments the relative proportion of unique and common elements and their control of the animals’ behavior was unknown. The experiments reported below aimed to re-assess the order of presentation and similarity interaction by using an improved procedure that allows for explicit control of the similarity between the target and the distractor (by adding common or distinctive elements, X and Y respectively) and accurate measure of the salience of the unique features of the target stimulus by using a sensory pre-conditioning sodium depletion procedure (e.g., Artigas et al., 2006; Dwyer et al., 2001; Dwyer and Mackintosh, 2002; Fudim, 1978; Symonds et al., 2002). In Experiment 1, four groups of rats were given serial exposure to two compound flavors. Animals in Group Forward-Similar were given exposure to Salt–X followed by AX whereas animals in Group Backward-Similar were given exposure to the same stimuli in the reversed order. Animals in Group Forward-Dissimilar were given exposure to Salt–X, followed by a distinctive compound consisting of two new elements, AY, whereas animals in Group Backward-Dissimilar were exposed to AY followed by Salt–X. The salience of the Salt element was then measured by assessing the capacity of Salt to enter into association with a novel flavor, N. After a single pairing between Salt and N (simultaneously presented in a compound, a sensory pre-conditioning procedure) the consumption of N was measured under a state of Salt need to be induced by an injection of FuroDoca. According to the Robertson and Garrud hypothesis, access of the target to the information processor would be prevented if it is preceded by a similar distractor. If that is correct, we should observe a pre-distractor effect when the target and the distractor are very similar; in the AX → Salt–X arrangement, the Salt element should remain highly salient. The same outcome should be observed when the target is followed by a dissimilar distractor (Salt–X → AY): the distractor would displace the target from the processor, and the Salt and X elements should remain highly salient. In the two remaining cases, (Salt–X → AX, the target prevents access of the distractor to the processor; and AY → Salt–X, the target displaces the distractor from the processor) the Salt element’s salience should be effectively decreased by pre-exposure.
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
2. Experiment 1 2.1. Method 2.1.1. Subjects and apparatus The subjects were 32 hooded Long Evans rats (Rattus norvegicus), 16 males (ad lib. body weight range: 306–401 g) and 16 females (ad lib. body weight range: 162–255 g), four months old at the start of the experiment and experimentally naïve. They were housed in individual cages in a colony room that was artificially lit from 9:00 a.m. to 9:00 p.m. daily. They were given continuous access to food, but access to water was restricted as detailed below. The solutions used as experimental stimuli were administered, in the home cages, at room temperature, in a 50-ml plastic centrifuge tube fitted with a rubber stopper and a stainless steel drinking spout. The following flavor solutions were used: A compound consisting of 1% w/v saline and 0.05% w/v citric acid, the Salt–X compound; a compound consisting of 1% vanilla solution (1%, v/v vanilla flavoring supplied by “Supercook”, Leeds, UK) and 0.05%, w/v of citric acid, the AX compound; a compound consisting of 1%, v/v of vanilla and 1%, w/v sucrose, the AY compound; a compound consisting of 1%, w/v saline and 0.5%, v/v almond solution (0.5%, v/v “Supercook” almond flavoring), the Salt–N compound; and a 0.5%, w/v almond solution, referred to in the text as N. Fluid consumption was measured by weighing the tubes. The treatment used to induce a sodium appetite was a subcutaneous injection of 0.5 ml of a mixture of 200 mg of furosemide (supplied by Sigma–Aldrich Quimica SA, Madrid, Spain) and 100 mg of deoxycorticosterone acetate (Sigma–Aldrich Quimica SA, Madrid, Spain) dispersed in 10 ml of distilled water with 1 drop of Tween 80 (Panreac Quimica SA, Barcelona, Spain). 2.1.2. Procedure The experiment started with a water deprivation schedule. The standard water bottles were first removed overnight. On the following four days, access to water was restricted: animals had access to water at 11:00 a.m. on day 1 for 2 h; on day 2 for 1.5 h; and on day 3 for 1 h. On day 4 animals were given access to water for 20 min at 11:00 a.m. and 4:00 p.m. Presentations of fluids continued to be given at these times throughout the experiment. During the next 3 days, animals were given access to water in the drinking tubes for 5 min at 11:00 a.m.; after 1 min delay, the animals were given 5 more minutes of access to water. This procedure was repeated in the p.m. session. On the last two days of this cycle, water intakes were measured, and subjects were assigned to four groups matched by levels of water consumption: the Forward-Similar, the Backward-Similar, the Forward-Dissimilar, and the BackwardDissimilar groups. Over the next 4 days, the pre-exposure phase, all the subjects received four serial trials in which two different compound flavors were presented (see Table 1). During the a.m. session of Day 1, animals in Group Forward-Similar were given access to a 3 ml sample of Salt–X for 5 min; after 1 min delay, animals were then given access to a 3 ml sample of AX for 5 min. All the animals drank the whole sample within the 5 min. The serial presentation of Salt–X followed by AX was repeated in the p.m. session of Day 1; animals had access to the fluids for 3 min with a delay of 1 min between the two compound flavors. This procedure was then replicated in the a.m. and the p.m. sessions of Days 2–4. Animals in Group BackwardSimilar were given serial trials in which access to AX was followed by access to Salt–X following the same procedure described for Group Forward-Similar. Animals in the Groups Forward-Dissimilar and Backward-Dissimilar were given forward and backward preexposure to Salt–X and AY. On the day following the final day of pre-exposure, all the animals were given access to 9 ml of the Salt–N compound at 11:00
Table 1 Experimental designs. Group Experiment 1 Forward-Similar Backward-Similar Forward-Dissimilar Backward-Dissimilar Experiment 2 Forward-Similar Backward-Similar Forward-Dissimilar Backward-Dissimilar
Pre-exposure
Conditioning
Test
Salt–X → AX AX → Salt–X Salt–X → AY AY → Salt–X
Salt–N Salt–N Salt–N Salt–N
(S. ap.) N (S. ap.) N (S. ap.) N (S. ap.) N
Salt–X → AX AX → Salt–X Salt → AX AX → Salt
Salt–N Salt–N Salt–N Salt–N
(S. ap.) N (S. ap.) N (S. ap.) N (S. ap.) N
Note: Salt, A, N, X and Y represent different flavors: Salt, saline solution; A, vanilla; N, almond; X, acid; and Y, sucrose. S. ap. represents the induction of a sodium appetite.
a.m. for 20 min, a sensory pre-conditioning procedure. Five hours later, all the animals received an injection of Furo-Doca. The food was then removed from the home cages in the colony room, and the subjects were given access to distilled water overnight. On the next day, the distilled water was removed from the cages 3 h prior to the test session. The test was initiated at noon and consisted of two 20-min sessions separated by a 30 min interval, in which the subjects had free access to flavor N (almond). 3. Results and discussion During the pre-exposure and the sensory pre-conditioning phases of the experiment, all the animals consumed all the fluid offered on each trial. Fig. 1 shows group means for consumption of N across the two test trials. An ANOVA with Order of Pre-exposure (Forward vs. Backward), Flavor (Similar vs. Dissimilar) and test showed a significant effect of test, F(1,28) = 7.92, and a significant Order × Flavor interaction, F(1,28) = 4.88. The remaining factors and interactions were all non-significant, maximum F(1,28) = 3.1. Further analyses of the Order × Flavor interaction, Simple Main Effects, showed that Group Forward-Similar consumed more of N than Group Backward-Similar, F(1,28) = 5.93. Groups ForwardDissimilar and Backward-Dissimilar show a similar consumption of the test flavor, F < 1. Also, Groups Forward (Similar and Dissimilar) showed a similar pattern of consumption during the test, F < 1. Finally, Group Backward-Similar consumed less of N during the test than Group Backward-Dissimilar, F(1,28) = 7.92. According to Robertson and Garrud (1983) interpretation of Wagner (1976) theory of stimuli processing, when two similar stimuli are used as the target and the distractor, a pre-distractor effect should be observed (AX → Salt–X, the distractor prevents the target from accessing the information processor). The present results challenge this interpretation: the salience of the unique
Forward-Similar Consumption in ml.
206
Backward-Similar
4
Forward-Dissimilar 3
Backward-Dissimilar
2 1 0
1
2
Test trials Fig. 1. Mean group consumption (±SE) of the N flavor over the two test trials of Experiment 1. Animals in the Similar groups were given exposure to Salt–X and AX; animals in the Dissimilar groups were given exposure to Salt–X and AY.
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
element Salt was better preserved when the Salt–X preceded the presentation of a similar AX stimulus (in the Forward condition) than when it followed AX (in the Backward condition). Robertson and Garrud (1983) would also predict that when the target is followed by a dissimilar distractor, Salt–X → AY, the salience of Salt should be preserved (the distractor displaces the target from the information processor). In the AY → Salt–X procedure, however, the distractor should be displaced by the target, and both the Salt and the X element should be well processed and hence habituated. Our results, however, revealed a preserved salience of the Salt element both in the forward and the backward conditions. Accordingly, the order of presentation of the target and the distractor seems to modulate habituation only when the two stimuli are very similar. When the two stimuli are dissimilar, the order of presentation seems to be irrelevant. An alternative way to explain the results observed in Experiments 1 would require us to focus on the relative low salience of the Salt element (reflected by poor consumption of N during the test) in the Backward-Similar group. Reduction in the salience of the Salt element seems to depend on presenting the Salt–X compound immediately after the AX compound. Presentation of AX should result in full activation of the A and X elements in A1. From the A1 state, elements are assumed to decay into the A2 state. And, according to Wagner (1981), any elements already in A2 will not be provoked to the primary state of activation in A1, even if the stimulus is again physically presented. Following this argumentation, presentation of AX would prevent full activation of X in A1 during the subsequent presentation of Salt–X, and the unique feature of the second compound, Salt, would be fully processed without having to compete with the common element. The unique feature of the first compound, A in the Backward and Salt in the Forward conditions, would be processed conjointly with the competing common element X; in that circumstance there would be less processing of the unique feature, and its salience or effectiveness would be better preserved than the salience of the unique feature of the second compound stimulus, an instance of overshadowing of habituation. This hypothesis could allow us to expect full processing of the Salt element when it is presented with an element whose representation has been primed by its presentation in the first compound in the Backward condition. We could also expect limited processing of the Salt element when it is presented in the first compound (Salt–X → AX; and Salt–X → AY), or in the second compound in the presence of a non-primed element (AY → Salt–X): in these arrangements the Salt element would have to compete for the limited processing resources with the X element. This would provide a comprehensive explanation of the results observed in Experiment 1. Furthermore, a prediction that can be derived from this view is that presenting the Salt element by itself either preceding or following another compound (e.g., AX) would result in full processing of this element (that would not have to compete with other elements), resulting in low salience of the Salt element and low consumption of N in the final test. Experiment 2 was designed to test this prediction.
4. Experiment 2 In Experiment 2 four groups of rats were given serial exposure to two different flavored solutions. Groups Forward-Similar and Backward-Similar were given exposure to the compound Salt–X followed by the compound AX and vice versa as in Experiment 1. Animals in Group Forward-Dissimilar were given exposure to Salt alone, followed by a distinctive compound consisting of two new elements, AX, whereas animals in Group BackwardDissimilar were exposed to AX followed by Salt. The salience of the Salt element was then measured by following the same procedure used in the previous experiment. According to the
207
hypothesis under assessment, the Salt element can be expected to be fully processed—and habituated—in the Backward-Similar group (AX → Salt–X, previous activation of X in A2 would prevent it from competing with the Salt element) as well as in the ForwardDissimilar and Backward-Dissimilar groups (in which the Salt is presented by itself). In the Forward-Similar group, however, the Salt element processing would be limited by its competence with the—fully activated in A1—common element X, and its salience can be expected to be relatively well preserved. Consumption of N in the test (which reflects the salience of the Salt element) should then be higher in the Forward-Similar than in the in Backward-Similar, Forward-Dissimilar and Backward-Dissimilar groups. 4.1. Method 4.1.1. Subjects and apparatus The subjects were 32 hooded Long Evans rats, 16 males (ad lib. body weight range: 246–337 g) and 16 females (ad lib. body weight range: 158–212 g), three months old at the start of the experiment and experimentally naïve. They were maintained in the same way and on the same water deprivation schedule as those used in the previous experiment. They were randomly assigned to four equal-sized groups (matched by sex and levels of water consumption): the Forward-Similar, the Backward-Similar, the Forward-Dissimilar and the Backward-Dissimilar groups. The flavors employed in Experiment 1 were used (Salt–X, AX, Salt–N, and N), as well as a 1%, w/v saline solution used in the Groups ForwardDissimilar and Backward-Dissimilar. Also, due to a mistake by the experimenter, this time we used a 1% almond solution (both in the Salt–N compound and in the N flavor) instead of the 0.5% solutions used in the previous experiment. 4.1.2. Procedure The experiment replicated the procedures used in Experiment 1. Animals in Group Forward-Similar, were given access to Salt–X followed by AX, whereas animals in Group Backward-Similar were given exposure to the same stimuli in the reversed order. Animals in Group Forward-Dissimilar were given serial trials in which access to Salt alone was followed by access to a completely different compound stimulus, AX. Finally, animals in Group Backward-Dissimilar were given access to AX followed by Salt. Following pre-exposure, the animals were given a sensory pre-conditioning trial with Salt–N, and were tested with N after the induction of a sodium appetite as in the previous experiment. 5. Results and discussion During the pre-exposure and the sensory pre-conditioning phases of the experiment, all the animals consumed all the fluid offered on each trial. Fig. 2 shows group means for consumption of N across the two test trials. An ANOVA with Order of Preexposure (Forward vs. Backward), Flavor (Similar vs. Dissimilar) and test showed a significant Test × Order × Flavor triple interaction, F(1,28) = 5.49. The remaining factors and interactions were all non-significant, maximum F(1,28) = 4.13. To further analyze the triple interaction, two ANOVAS with Order and Flavor as the factors were carried out taking into account the data from Test 1 and Test 2 respectively. The analysis of the first test trial showed a significant Order × Flavor interaction, F(1,28) = 5,39). The main effects did not reach the level of significance, Fs(1,28) ≤ 2.00. Further analyses of the Order × Flavor interaction, Simple Main Effects, showed that Group Forward-Similar consumed more of N than Group Backward-Similar, F(1,28) = 6.53. Groups Forward-Dissimilar and Backward-Dissimilar showed a similar consumption of the test flavor, F < 1. Group Forward-Similar significantly drank more of N than Group Forward-Dissimilar, F(1,28) = 6.98. Finally, the two Backward
208
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
Consumption in ml.
Forward-Similar
Backward-Similar
4
Forward-Dissimilar
3
Backward-Dissimilar
2 1 0
1
2
Test trials Fig. 2. Mean group consumption (±SE) of the N flavor over the two test trials of Experiment 2. Animals in the Similar groups were given exposure to Salt–X and AX; animals in the Dissimilar groups were given exposure to Salt and AX.
(Similar and Dissimilar) groups did not differ, F < 1. The analysis of the second test trial did not show any significant factor effect or interaction, Fs < 1. The results of Experiment 2 seem to confirm the hypothesis under assessment: the relative low consumption of N during the final test trial in Groups Backward-Similar, Forward-Dissimilar and Backward-Dissimilar can be taken to reflect similar full processing of the Salt element that resulted in high habituation of this element. In contrast, higher consumption of N (which reflects high salience of the Salt element) in Group Forward-Similar seems to suggest that the processing of the Salt element in the first compound was limited by the presence of a fully activated competitor, X. 6. General discussion In two experiments, rats were given serial exposure to compound flavored solutions that contained unique and common features. Following pre-exposure, one of the unique features (always a saline solution) was presented in a compound with a novel flavor, N. The salience or effectiveness of the salted unique feature was then assessed by presenting the new flavor, N, under a state of Salt appetite induced by an injection of Furo-Doca. In Experiment 1, animals were given exposure trials to Salt–X (a saline-acid compound) which could be followed or preceded by presentation of a similar distractor, AX, or by a dissimilar distractor, AY. The order of presentation was found to modulate the effect of pre-exposure upon the salience of the unique feature of the target stimulus (Salt) only when the distractor was a similar stimulus: the Salt element was more salient after forward (the target followed by the distractor, Salt–X → AX) than backward pre-exposure (the distractor followed by the target, AX → Salt–X). In the groups in which the target was presented along with a dissimilar distractor, no effect of the order of presentation (forward and backward) was observed; in both conditions, the salience of the Salt element was preserved as in the Forward-Similar condition. Experiment 2 replicated the procedure used in Experiment 1 concerning the Groups Similar (Forward and Backward). In the groups Dissimilar, however, animals were pre-exposed to the Salt element alone, followed by a dissimilar compound stimulus, AX. The results replicated the order effect observed in the groups Similar of Experiment 1: the salience of the Salt element was better preserved in the Forward than in the Backward group. In the groups Dissimilar (exposed to Salt alone) the salience of the Salt element was reduced as in the BackwardSimilar condition. According to the literature on distractor effects (e.g., Robertson and Garrud, 1983; Shanks et al., 1986), low habituation of the target could be attributed to an interruption of its processing in a limited capacity device due to the presentation closely in time of the
distractor. Robertson and Garrud (1983) explained the distractor effects upon habituation by using a version of the well known Wagner’s theory of memory and habituation (1976, 1981). The main hypothesis stated that access to the limited capacity information processor could be prevented if a similar stimulus was being processed. According to Robertson and Garrud, an order effect should be observed when using similar target and distractor stimuli. When the target is followed by a similar distractor (Salt–X followed by AX), the distractor would not gain access to the processor, and full processing of the target will result in full habituation of its unique and common features (Salt and X). In the backward order (AX → Salt–X), the target stimulus will not gain access to the information processor, and low habituation of the Salt element should be detected (the X element, present in the first compound, should be subject to habituation). Our results showed the opposite pattern of results: the Salt element was more salient after forward than backward pre-exposure. Robertson and Garrud (1983) also predict an order effect when the target and the distractor are dissimilar: when a target is followed by a dissimilar distractor (Salt–X → AY) the distractor should displace the target from the processor and its elements (Salt and X) should retain their salience or effectiveness. In the backward arrangement (AY → Salt–X), the target would displace the distractor from the processor, and processing of the target will result in full habituation of its unique and common features (Salt and X). Experiment 1 revealed, however, an equally preserved salience of the unique element Salt in the forward and the backward arrangements. So no evidence could be found to support the Robertson and Garrud (1983) hypothesis. At this point, we decided to focus our attention on the only group in which the salience of the unique feature Salt was significantly reduced during the pre-exposure phase: the Backward-Similar condition in which the animals were exposed to AX immediately followed by Salt–X. Assuming the principles of Wagner’s SOP model, we hypothesized that the presence of X in the first compound should result in full activation of the representation of this event. However, after a short delay, this activation would decay into a less effective or marginal A2 state of activation that prevents further activation into A1 even if the stimulus is physically presented again. That being the case, the Salt element in the second compound could be expected to be fully processed (and habituated), given that the potentially competing common element X would be in a state of marginal activation. This hypothesis can successfully account for the results observed in Experiment 1 of the present study. Furthermore, one prediction that could be derived from that hypothesis was that presenting the Salt element by itself (either in the Forward-Dissimilar or the Backward-Dissimilar condition) should result in full processing of that stimulus equivalent to the processing in the Backward-Similar condition. Experiment 2 confirmed the accuracy of this prediction. This pattern of results extends and complements the existent literature on distractor effects. Kaye et al. (1988) suggested that the similarity between the target and the distractor could account for the absence of a distractor effect either when the animals were given forward (the target followed by the distractor) or backward (the distractor followed by the target) pre-exposure. In both cases, the habituation of the common element X should generalize from the distractor to the target at the time of test, counteracting any distractor effect due to interruption of processing. However, this view overlooked the possible changes in the salience or effectiveness of the unique features of the target and the distractor: at the time of test, the net response observed would be controlled by the common elements, hindering any effect attributable to the salience or effectiveness of the unique features. In our research, we have gone a step further by assessing the effect of the order of presentation of the target and the distractor upon the habituation of the unique feature of the target stimulus. The present experiments have shown
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
that serial exposure to similar stimuli protects the salience of the unique features of the compound presented first. Taken together, the Kaye et al.’s study and the present results suggest that two mechanisms modulate the distractor effects: a Wagner’s like mechanism that protects the salience of some features of the pre-exposed compound stimuli, and the generalization of habituation between stimuli sharing a significant proportion of common elements. To conclude, the learning mechanism characterized in the present experiments seems to be adequate to account for distractor effects; more generally, it informs about the way in which similar stimuli presented closely in time are processed. References Artigas, A.A., Sansa, J., Blair, C.A.J., Hall, G., Prados, J., 2006. Enhanced discrimination between flavor stimuli: roles of salience modulation and inhibition. Journal of Experimental Psychology: Animal Behavior Processes 32, 173–177. Atkinson, R.C., Shiffrin, R.M., 1968. Human memory: a proposed system and its control processes. In: Spence, K.W., Spence, J.T. (Eds.), The Psychology of Learning and Motivation (vol. 2). Academic Press, New York, pp. 89–195. Dwyer, D.M., Bennett, C.H., Mackintosh, N.J., 2001. Evidence for inhibitory associations between the unique elements of two compound flavours. Quarterly Journal of Experimental Psychology 54B, 97–107. Dwyer, D.M., Mackintosh, N.J., 2002. Alternating exposure to two compound flavors creates inhibitory associations between their unique features. Animal Learning and Behavior 30, 177–200.
209
Fudim, O.K., 1978. Sensory preconditioning of flavors with a formalin-produced sodium need. Journal of Experimental Psychology: Animal Behavior Processes 4, 276–285. Green, K.F., Parker, L.A., 1975. Gustatory memory: incubation and interference. Behavioral Biology 13, 359–367. Kaye, H., Swietalski, N., Mackintosh, N.J., 1988. Habituation as a function of similarity and temporal location of target and distractor stimuli. Animal Learning & Behavior 16, 93–99. Rankin, C.H., Abrams, T., Barry, R.J., Bhatnagar, S., Clayton, D.F., Colombo, J., Coppola, G., Geyer, M.A., Glanzman, D.L., Marsland, S., Mcsweeney, F.K., Wilson, D.A., Wu, C., Thompson, R.F., 2009. Habituation revisited: an updated and revised description of the behavioural characteristics of habituation. Neurobiology of Learning and Memory 92, 135–138. Robertson, D., Garrud, P., 1983. Variable processing of flavours in rat STM. Animal Learning & Behavior 11, 474–482. Shanks, D.R., Preston, G.C., Stanhope, K.J., 1986. Effects of distractor familiarity on habituation of neophobia. Animal Learning & Behavior 14, 393–397. Symonds, M., Hall, G., Bailey, G.K., 2002. Perceptual learning with a sodium depletion procedure. Journal of Experimental Psychology: Animal Behavior Processes 28, 190–199. Thompson, R.F., Spencer, W.A., 1966. Habituation: a model phenomenon for the study of neuronal substrates of behaviour. Psychological Review 173, 16–43. Wagner, A.R., 1976. Priming in STM: an information-processing mechanism for self-generated or retrieval-generated depression in performance. In: Tighe, T.J., Leaton, R.N. (Eds.), Habituation: Perspectives From Child Development, Animal Behavior, and Neuropsychology. Lawrence Erlbaum Associates, Inc., Hillsdale, NJ, pp. 95–128. Wagner, A.R., 1981. SOP: a model of automatic memory processing in animal behavior. In: Spear, N.E., Miller, R.R. (Eds.), Information Processing in Animals: Memory Mechanisms. Lawrence Erlbaum Associates, Inc., Hillsdale, NJ, pp. 5–47.
Contents lists available at SciVerse ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Distractor effects upon habituation of complex stimuli夽 Antonio A. Artigas a,b,∗∗ , Joan Sansa a,b , Jose Prados c,∗ a
Departament de Psicologia Bàsica, Universitat de Barcelona, Spain Institut de Recerca en Cervell, Conducta i Cognicio, IR3C Barcelona, Spain c School of Psychology, University of Leicester, University Road, LE1 9HN Leicester, United Kingdom b
a r t i c l e
i n f o
Article history: Received 12 July 2011 Received in revised form 16 December 2011 Accepted 26 January 2012 Keywords: Distractor effects Generalization decrement Wagner’s SOP theory
a b s t r a c t In two experiments, rats were given serial forward (the target followed by the distractor) or backward (the distractor followed by the target) exposure to two compound flavor stimuli that could be either similar (Salt–X/AX) or dissimilar (Salt–X/AY, Experiment 1; Salt/AX, Experiment 2). Following pre-exposure, the Salt element was presented in a compound with a novel flavor, N. The salience or effectiveness of the Salt element was then assessed by presenting the new flavor, N, under a state of salt appetite. Experiments 1 and 2 revealed that the order of presentation modulated the habituation of the Salt element only when the distractor was similar to the target: the Salt element was more salient after forward than backward pre-exposure. In the groups Dissimilar the order of pre-exposure was irrelevant; however, when the Salt element was presented in compound with a second element (Salt–X, Experiment 1), its salience was preserved, whereas when it was presented alone (Salt, Experiment 2) its salience was significantly reduced. These results, which are discussed in terms of Wagner (1981) theory of habituation, inform about the way in which stimuli presented closely in time are processed. © 2012 Elsevier B.V. All rights reserved.
1. Distractor effects upon habituation of complex stimuli Non-reinforced exposure to stimuli has been shown to affect the way in which they can control an animal’s behavior. For example, repeated presentations of a stimulus result in a loss of its salience or perceptual effectiveness, declining the strength of any responses it initially elicited—a process of habituation (e.g., Rankin et al., 2009; Thompson and Spencer, 1966). Such habituation, however, can be disrupted by the presentation of an additional stimulus or distractor closely in time (e.g., Green and Parker, 1975; Shanks et al., 1986; Thompson and Spencer, 1966). Several factors have been found to modulate the distractor effect: the similarity between the target and the distractor (e.g., Robertson and Garrud, 1983; Kaye et al., 1988); and the order of presentation of the target and the distractor (e.g., Robertson and Garrud, 1983). In the study by Robertson and Garrud (1983), rats were given one exposure trial to a particular flavor and the habituation of its neophobia—the natural response of rats to new flavor stimuli—was then assessed. Disruption of habituation was observed when the
夽 This work was supported by a grant from the Spanish Ministerio de Ciencia e Innovación (Ref: SEJ2007-67416) to the authors. ∗ Corresponding author at: School of Psychology, University of Leicester, Lancaster Road, LE1 9HN Leicester, United Kingdom. Tel.: +44 116 2297150; fax: +44 116 2297196. ∗∗ Corresponding author at: Departament de Psicologia Bàsica, Universitat de Barcelona, Pg. de la Vall d’Hebron 171, 08035-Barcelona, Spain. E-mail addresses: [email protected] (A.A. Artigas), [email protected] (J. Prados). 0376-6357/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2012.01.009
target flavor was followed by a dissimilar stimulus (sucrose followed by coffee, a post-distractor effect), but not when the target was followed by a similar distractor (lemon followed by coffee). Interestingly, when they reversed the order in a second experiment, the pattern of results was also reversed: disruption of habituation was observed when the target was preceded by a similar stimulus (coffee preceded by lemon, a pre-distractor effect), but not when it was preceded by a dissimilar distractor (coffee preceded by sucrose). (Robertson & Garrud presented independent evidence that the similarity between coffee and lemon was higher than the similarity between coffee and sucrose.) To account for this intriguing pattern of results, Robertson and Garrud (1983) offered an explanation based on Wagner (1976, 1981) theory of stimulus processing. The theory assumes that habituation depends on how well stimuli are processed in a limitedcapacity short term memory (STM) unit, and distinguishes between two activation states in the STM. Presentation of a stimulus would result in full activation of the stimulus in the STM unit—the A1 state in which the stimulus will be fully processed. Subsequently, activation would decay into a marginal level of activation—the A2 state in which the stimulus is active but subject to limited processing (Atkinson and Shiffrin, 1968; Wagner, 1981). Interestingly, any elements already in A2 will not be provoked to the primary state of activation in A1, even if the stimulus is again physically presented. According to Robertson and Garrud (1983), this would also apply for a similar stimulus: if stimulus X is in A2, presentation a very similar stimulus, X’, would not result in its activation in A1 in the STM unit, and stimulus X’ would not be processed. However, serial
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
presentation of two distinctive stimuli (X and Y) would result in the second one displacing the first one from the capacity limited STM unit, resulting in good processing of the second but not the first event. Going back to the Robertson and Garrud (1983) experiments, when the target flavor is immediately followed by a distinctive distractor, the target would be displaced from STM and its processing would be interrupted. However, when a very similar distractor follows the presentation of the target, access to the STM unit by the distractor would be prevented, and the target would be fully processed. That would explain why a post-distractor effect can only be observed when the target and the distractor are dissimilar. On the other hand, a dissimilar target would be able to displace a predistractor from the STM unit, and full processing of the target would result in normal habituation; however, a similar pre-distractor would prevent the access of the target to the STM unit, disrupting the habituation process. This could account for the pre-distractor effect that was observed when the target and the distractor were very similar. Kaye et al. (1988) pointed out that the effect observed by Robertson & Garrud with a similar pre-distractor is a surprising outcome. Even assuming that a similar pre-distractor could prevent the access of the target to the capacity-limited processor, this should be counteracted by the generalization of the habituation acquired by the distractor to the target. Kaye et al. carried out a series of experiments which aimed to directly assess the interaction between the order of presentation and the similarity between the target and the distractor reported by Robertson and Garrud (1983). In one of the experiments reported by Kaye et al., animals were given exposure to a target lemon flavor stimulus. When lemon was preceded or followed by the presentation of a dissimilar saline solution, significant disruption of habituation to the target lemon flavor was observed. However, when the lemon flavor was preceded or followed by the presentation of a similar flavor, coffee, habituation proceeded almost normally (Kaye et al., 1988, presented independent evidence that the coffee stimulus was salient enough to disrupt habituation of other dissimilar stimuli, like a saline-sucrose mixed solution; and that coffee was more similar to lemon than the saline solution.) The results reported by Kaye et al. (1988) suggest that the similarity between the target and the distractor modulates the distractor effects; the order of presentation, however, was found to be irrelevant. The authors of the study proposed an explanation of the distractor effects based on the generalization decrement principle. Exposure (in any order) to two flavor stimuli can be said to involve exposure to their unique features (A and B, where A represents what is unique to lemon, and B what is unique to coffee, for example) as well as exposure to their common elements (X). The proportion of X common elements will vary according to the similarity of the two stimuli: we can expect the proportion of X elements to be higher when using similar flavors—lemon and coffee—than when using dissimilar flavors—lemon and sucrose. In the case in which the two stimuli are very similar, we could assume that habituation to AX will generalize to BX via X. In the case in which the target and the distractor are dissimilar, we can expect this generalization to be lower (because the low proportion of common elements). And this is the outcome that was observed in the experiments reported by Kaye et al. (1988). There is, however a limitation in the analysis carried out by Kaye et al. (1988): whatever happens in the test will depend on the habituation to the common elements, X; but differences in the habituation to the unique features of two similar stimuli (A, what is unique to lemon; and B, what is unique to coffee) would be masked by the habituation acquired by the common elements. In fact, there are reasons to believe that the order of exposure to the target and the distractor could have an effect upon the habituation
205
to the unique elements A and B. Going back to the explanation proposed by Robertson and Garrud (1983) for the distractor effects, if two similar stimuli are presented within a short period of time, the first stimulus to gain access to the STM unit would prevent the access to the processor of the other one. If the target stimulus is presented first (AX → BX), both its unique and common features (A and X) would be adequately processed, resulting in full habituation; and only the unique features of the distractor (B) would remain intact—because they get no access to the processor. However, if the target follows the distractor (BX → AX) its unique features (A) would remain intact. That being the case, a salient A element presented in compound with a habituated X element could control the performance of the individual during the test, resulting in a pre-distractor effect (as observed in the experiments by Robertson and Garrud, 1983). If two dissimilar stimuli are used (the target AX and the distractor BY), the opposite pattern of results could be expected. In the AX → BY arrangement (the target followed by the distractor), the distractor would displace the target from the capacity-limited STM unit. In that way, A and X would remain intact, resulting in a post-distractor effect. However, in the BY → AX arrangement is the target who displaces the distractor from the STM unit, ensuring full processing of its elements, A and X. This would result in habituation of all the elements of the target AX (absence of a pre-distractor effect). And this is exactly what Robertson and Garrud observed in their experiments. The experiments reported by Robertson and Garrud (1983) and Kaye et al. (1988) seem to suggest the action of two different mechanisms that modulate the habituation of the elements of the pre-exposed flavors. However, it is difficult to ascertain how these mechanisms work because in their experiments the relative proportion of unique and common elements and their control of the animals’ behavior was unknown. The experiments reported below aimed to re-assess the order of presentation and similarity interaction by using an improved procedure that allows for explicit control of the similarity between the target and the distractor (by adding common or distinctive elements, X and Y respectively) and accurate measure of the salience of the unique features of the target stimulus by using a sensory pre-conditioning sodium depletion procedure (e.g., Artigas et al., 2006; Dwyer et al., 2001; Dwyer and Mackintosh, 2002; Fudim, 1978; Symonds et al., 2002). In Experiment 1, four groups of rats were given serial exposure to two compound flavors. Animals in Group Forward-Similar were given exposure to Salt–X followed by AX whereas animals in Group Backward-Similar were given exposure to the same stimuli in the reversed order. Animals in Group Forward-Dissimilar were given exposure to Salt–X, followed by a distinctive compound consisting of two new elements, AY, whereas animals in Group Backward-Dissimilar were exposed to AY followed by Salt–X. The salience of the Salt element was then measured by assessing the capacity of Salt to enter into association with a novel flavor, N. After a single pairing between Salt and N (simultaneously presented in a compound, a sensory pre-conditioning procedure) the consumption of N was measured under a state of Salt need to be induced by an injection of FuroDoca. According to the Robertson and Garrud hypothesis, access of the target to the information processor would be prevented if it is preceded by a similar distractor. If that is correct, we should observe a pre-distractor effect when the target and the distractor are very similar; in the AX → Salt–X arrangement, the Salt element should remain highly salient. The same outcome should be observed when the target is followed by a dissimilar distractor (Salt–X → AY): the distractor would displace the target from the processor, and the Salt and X elements should remain highly salient. In the two remaining cases, (Salt–X → AX, the target prevents access of the distractor to the processor; and AY → Salt–X, the target displaces the distractor from the processor) the Salt element’s salience should be effectively decreased by pre-exposure.
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
2. Experiment 1 2.1. Method 2.1.1. Subjects and apparatus The subjects were 32 hooded Long Evans rats (Rattus norvegicus), 16 males (ad lib. body weight range: 306–401 g) and 16 females (ad lib. body weight range: 162–255 g), four months old at the start of the experiment and experimentally naïve. They were housed in individual cages in a colony room that was artificially lit from 9:00 a.m. to 9:00 p.m. daily. They were given continuous access to food, but access to water was restricted as detailed below. The solutions used as experimental stimuli were administered, in the home cages, at room temperature, in a 50-ml plastic centrifuge tube fitted with a rubber stopper and a stainless steel drinking spout. The following flavor solutions were used: A compound consisting of 1% w/v saline and 0.05% w/v citric acid, the Salt–X compound; a compound consisting of 1% vanilla solution (1%, v/v vanilla flavoring supplied by “Supercook”, Leeds, UK) and 0.05%, w/v of citric acid, the AX compound; a compound consisting of 1%, v/v of vanilla and 1%, w/v sucrose, the AY compound; a compound consisting of 1%, w/v saline and 0.5%, v/v almond solution (0.5%, v/v “Supercook” almond flavoring), the Salt–N compound; and a 0.5%, w/v almond solution, referred to in the text as N. Fluid consumption was measured by weighing the tubes. The treatment used to induce a sodium appetite was a subcutaneous injection of 0.5 ml of a mixture of 200 mg of furosemide (supplied by Sigma–Aldrich Quimica SA, Madrid, Spain) and 100 mg of deoxycorticosterone acetate (Sigma–Aldrich Quimica SA, Madrid, Spain) dispersed in 10 ml of distilled water with 1 drop of Tween 80 (Panreac Quimica SA, Barcelona, Spain). 2.1.2. Procedure The experiment started with a water deprivation schedule. The standard water bottles were first removed overnight. On the following four days, access to water was restricted: animals had access to water at 11:00 a.m. on day 1 for 2 h; on day 2 for 1.5 h; and on day 3 for 1 h. On day 4 animals were given access to water for 20 min at 11:00 a.m. and 4:00 p.m. Presentations of fluids continued to be given at these times throughout the experiment. During the next 3 days, animals were given access to water in the drinking tubes for 5 min at 11:00 a.m.; after 1 min delay, the animals were given 5 more minutes of access to water. This procedure was repeated in the p.m. session. On the last two days of this cycle, water intakes were measured, and subjects were assigned to four groups matched by levels of water consumption: the Forward-Similar, the Backward-Similar, the Forward-Dissimilar, and the BackwardDissimilar groups. Over the next 4 days, the pre-exposure phase, all the subjects received four serial trials in which two different compound flavors were presented (see Table 1). During the a.m. session of Day 1, animals in Group Forward-Similar were given access to a 3 ml sample of Salt–X for 5 min; after 1 min delay, animals were then given access to a 3 ml sample of AX for 5 min. All the animals drank the whole sample within the 5 min. The serial presentation of Salt–X followed by AX was repeated in the p.m. session of Day 1; animals had access to the fluids for 3 min with a delay of 1 min between the two compound flavors. This procedure was then replicated in the a.m. and the p.m. sessions of Days 2–4. Animals in Group BackwardSimilar were given serial trials in which access to AX was followed by access to Salt–X following the same procedure described for Group Forward-Similar. Animals in the Groups Forward-Dissimilar and Backward-Dissimilar were given forward and backward preexposure to Salt–X and AY. On the day following the final day of pre-exposure, all the animals were given access to 9 ml of the Salt–N compound at 11:00
Table 1 Experimental designs. Group Experiment 1 Forward-Similar Backward-Similar Forward-Dissimilar Backward-Dissimilar Experiment 2 Forward-Similar Backward-Similar Forward-Dissimilar Backward-Dissimilar
Pre-exposure
Conditioning
Test
Salt–X → AX AX → Salt–X Salt–X → AY AY → Salt–X
Salt–N Salt–N Salt–N Salt–N
(S. ap.) N (S. ap.) N (S. ap.) N (S. ap.) N
Salt–X → AX AX → Salt–X Salt → AX AX → Salt
Salt–N Salt–N Salt–N Salt–N
(S. ap.) N (S. ap.) N (S. ap.) N (S. ap.) N
Note: Salt, A, N, X and Y represent different flavors: Salt, saline solution; A, vanilla; N, almond; X, acid; and Y, sucrose. S. ap. represents the induction of a sodium appetite.
a.m. for 20 min, a sensory pre-conditioning procedure. Five hours later, all the animals received an injection of Furo-Doca. The food was then removed from the home cages in the colony room, and the subjects were given access to distilled water overnight. On the next day, the distilled water was removed from the cages 3 h prior to the test session. The test was initiated at noon and consisted of two 20-min sessions separated by a 30 min interval, in which the subjects had free access to flavor N (almond). 3. Results and discussion During the pre-exposure and the sensory pre-conditioning phases of the experiment, all the animals consumed all the fluid offered on each trial. Fig. 1 shows group means for consumption of N across the two test trials. An ANOVA with Order of Pre-exposure (Forward vs. Backward), Flavor (Similar vs. Dissimilar) and test showed a significant effect of test, F(1,28) = 7.92, and a significant Order × Flavor interaction, F(1,28) = 4.88. The remaining factors and interactions were all non-significant, maximum F(1,28) = 3.1. Further analyses of the Order × Flavor interaction, Simple Main Effects, showed that Group Forward-Similar consumed more of N than Group Backward-Similar, F(1,28) = 5.93. Groups ForwardDissimilar and Backward-Dissimilar show a similar consumption of the test flavor, F < 1. Also, Groups Forward (Similar and Dissimilar) showed a similar pattern of consumption during the test, F < 1. Finally, Group Backward-Similar consumed less of N during the test than Group Backward-Dissimilar, F(1,28) = 7.92. According to Robertson and Garrud (1983) interpretation of Wagner (1976) theory of stimuli processing, when two similar stimuli are used as the target and the distractor, a pre-distractor effect should be observed (AX → Salt–X, the distractor prevents the target from accessing the information processor). The present results challenge this interpretation: the salience of the unique
Forward-Similar Consumption in ml.
206
Backward-Similar
4
Forward-Dissimilar 3
Backward-Dissimilar
2 1 0
1
2
Test trials Fig. 1. Mean group consumption (±SE) of the N flavor over the two test trials of Experiment 1. Animals in the Similar groups were given exposure to Salt–X and AX; animals in the Dissimilar groups were given exposure to Salt–X and AY.
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
element Salt was better preserved when the Salt–X preceded the presentation of a similar AX stimulus (in the Forward condition) than when it followed AX (in the Backward condition). Robertson and Garrud (1983) would also predict that when the target is followed by a dissimilar distractor, Salt–X → AY, the salience of Salt should be preserved (the distractor displaces the target from the information processor). In the AY → Salt–X procedure, however, the distractor should be displaced by the target, and both the Salt and the X element should be well processed and hence habituated. Our results, however, revealed a preserved salience of the Salt element both in the forward and the backward conditions. Accordingly, the order of presentation of the target and the distractor seems to modulate habituation only when the two stimuli are very similar. When the two stimuli are dissimilar, the order of presentation seems to be irrelevant. An alternative way to explain the results observed in Experiments 1 would require us to focus on the relative low salience of the Salt element (reflected by poor consumption of N during the test) in the Backward-Similar group. Reduction in the salience of the Salt element seems to depend on presenting the Salt–X compound immediately after the AX compound. Presentation of AX should result in full activation of the A and X elements in A1. From the A1 state, elements are assumed to decay into the A2 state. And, according to Wagner (1981), any elements already in A2 will not be provoked to the primary state of activation in A1, even if the stimulus is again physically presented. Following this argumentation, presentation of AX would prevent full activation of X in A1 during the subsequent presentation of Salt–X, and the unique feature of the second compound, Salt, would be fully processed without having to compete with the common element. The unique feature of the first compound, A in the Backward and Salt in the Forward conditions, would be processed conjointly with the competing common element X; in that circumstance there would be less processing of the unique feature, and its salience or effectiveness would be better preserved than the salience of the unique feature of the second compound stimulus, an instance of overshadowing of habituation. This hypothesis could allow us to expect full processing of the Salt element when it is presented with an element whose representation has been primed by its presentation in the first compound in the Backward condition. We could also expect limited processing of the Salt element when it is presented in the first compound (Salt–X → AX; and Salt–X → AY), or in the second compound in the presence of a non-primed element (AY → Salt–X): in these arrangements the Salt element would have to compete for the limited processing resources with the X element. This would provide a comprehensive explanation of the results observed in Experiment 1. Furthermore, a prediction that can be derived from this view is that presenting the Salt element by itself either preceding or following another compound (e.g., AX) would result in full processing of this element (that would not have to compete with other elements), resulting in low salience of the Salt element and low consumption of N in the final test. Experiment 2 was designed to test this prediction.
4. Experiment 2 In Experiment 2 four groups of rats were given serial exposure to two different flavored solutions. Groups Forward-Similar and Backward-Similar were given exposure to the compound Salt–X followed by the compound AX and vice versa as in Experiment 1. Animals in Group Forward-Dissimilar were given exposure to Salt alone, followed by a distinctive compound consisting of two new elements, AX, whereas animals in Group BackwardDissimilar were exposed to AX followed by Salt. The salience of the Salt element was then measured by following the same procedure used in the previous experiment. According to the
207
hypothesis under assessment, the Salt element can be expected to be fully processed—and habituated—in the Backward-Similar group (AX → Salt–X, previous activation of X in A2 would prevent it from competing with the Salt element) as well as in the ForwardDissimilar and Backward-Dissimilar groups (in which the Salt is presented by itself). In the Forward-Similar group, however, the Salt element processing would be limited by its competence with the—fully activated in A1—common element X, and its salience can be expected to be relatively well preserved. Consumption of N in the test (which reflects the salience of the Salt element) should then be higher in the Forward-Similar than in the in Backward-Similar, Forward-Dissimilar and Backward-Dissimilar groups. 4.1. Method 4.1.1. Subjects and apparatus The subjects were 32 hooded Long Evans rats, 16 males (ad lib. body weight range: 246–337 g) and 16 females (ad lib. body weight range: 158–212 g), three months old at the start of the experiment and experimentally naïve. They were maintained in the same way and on the same water deprivation schedule as those used in the previous experiment. They were randomly assigned to four equal-sized groups (matched by sex and levels of water consumption): the Forward-Similar, the Backward-Similar, the Forward-Dissimilar and the Backward-Dissimilar groups. The flavors employed in Experiment 1 were used (Salt–X, AX, Salt–N, and N), as well as a 1%, w/v saline solution used in the Groups ForwardDissimilar and Backward-Dissimilar. Also, due to a mistake by the experimenter, this time we used a 1% almond solution (both in the Salt–N compound and in the N flavor) instead of the 0.5% solutions used in the previous experiment. 4.1.2. Procedure The experiment replicated the procedures used in Experiment 1. Animals in Group Forward-Similar, were given access to Salt–X followed by AX, whereas animals in Group Backward-Similar were given exposure to the same stimuli in the reversed order. Animals in Group Forward-Dissimilar were given serial trials in which access to Salt alone was followed by access to a completely different compound stimulus, AX. Finally, animals in Group Backward-Dissimilar were given access to AX followed by Salt. Following pre-exposure, the animals were given a sensory pre-conditioning trial with Salt–N, and were tested with N after the induction of a sodium appetite as in the previous experiment. 5. Results and discussion During the pre-exposure and the sensory pre-conditioning phases of the experiment, all the animals consumed all the fluid offered on each trial. Fig. 2 shows group means for consumption of N across the two test trials. An ANOVA with Order of Preexposure (Forward vs. Backward), Flavor (Similar vs. Dissimilar) and test showed a significant Test × Order × Flavor triple interaction, F(1,28) = 5.49. The remaining factors and interactions were all non-significant, maximum F(1,28) = 4.13. To further analyze the triple interaction, two ANOVAS with Order and Flavor as the factors were carried out taking into account the data from Test 1 and Test 2 respectively. The analysis of the first test trial showed a significant Order × Flavor interaction, F(1,28) = 5,39). The main effects did not reach the level of significance, Fs(1,28) ≤ 2.00. Further analyses of the Order × Flavor interaction, Simple Main Effects, showed that Group Forward-Similar consumed more of N than Group Backward-Similar, F(1,28) = 6.53. Groups Forward-Dissimilar and Backward-Dissimilar showed a similar consumption of the test flavor, F < 1. Group Forward-Similar significantly drank more of N than Group Forward-Dissimilar, F(1,28) = 6.98. Finally, the two Backward
208
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
Consumption in ml.
Forward-Similar
Backward-Similar
4
Forward-Dissimilar
3
Backward-Dissimilar
2 1 0
1
2
Test trials Fig. 2. Mean group consumption (±SE) of the N flavor over the two test trials of Experiment 2. Animals in the Similar groups were given exposure to Salt–X and AX; animals in the Dissimilar groups were given exposure to Salt and AX.
(Similar and Dissimilar) groups did not differ, F < 1. The analysis of the second test trial did not show any significant factor effect or interaction, Fs < 1. The results of Experiment 2 seem to confirm the hypothesis under assessment: the relative low consumption of N during the final test trial in Groups Backward-Similar, Forward-Dissimilar and Backward-Dissimilar can be taken to reflect similar full processing of the Salt element that resulted in high habituation of this element. In contrast, higher consumption of N (which reflects high salience of the Salt element) in Group Forward-Similar seems to suggest that the processing of the Salt element in the first compound was limited by the presence of a fully activated competitor, X. 6. General discussion In two experiments, rats were given serial exposure to compound flavored solutions that contained unique and common features. Following pre-exposure, one of the unique features (always a saline solution) was presented in a compound with a novel flavor, N. The salience or effectiveness of the salted unique feature was then assessed by presenting the new flavor, N, under a state of Salt appetite induced by an injection of Furo-Doca. In Experiment 1, animals were given exposure trials to Salt–X (a saline-acid compound) which could be followed or preceded by presentation of a similar distractor, AX, or by a dissimilar distractor, AY. The order of presentation was found to modulate the effect of pre-exposure upon the salience of the unique feature of the target stimulus (Salt) only when the distractor was a similar stimulus: the Salt element was more salient after forward (the target followed by the distractor, Salt–X → AX) than backward pre-exposure (the distractor followed by the target, AX → Salt–X). In the groups in which the target was presented along with a dissimilar distractor, no effect of the order of presentation (forward and backward) was observed; in both conditions, the salience of the Salt element was preserved as in the Forward-Similar condition. Experiment 2 replicated the procedure used in Experiment 1 concerning the Groups Similar (Forward and Backward). In the groups Dissimilar, however, animals were pre-exposed to the Salt element alone, followed by a dissimilar compound stimulus, AX. The results replicated the order effect observed in the groups Similar of Experiment 1: the salience of the Salt element was better preserved in the Forward than in the Backward group. In the groups Dissimilar (exposed to Salt alone) the salience of the Salt element was reduced as in the BackwardSimilar condition. According to the literature on distractor effects (e.g., Robertson and Garrud, 1983; Shanks et al., 1986), low habituation of the target could be attributed to an interruption of its processing in a limited capacity device due to the presentation closely in time of the
distractor. Robertson and Garrud (1983) explained the distractor effects upon habituation by using a version of the well known Wagner’s theory of memory and habituation (1976, 1981). The main hypothesis stated that access to the limited capacity information processor could be prevented if a similar stimulus was being processed. According to Robertson and Garrud, an order effect should be observed when using similar target and distractor stimuli. When the target is followed by a similar distractor (Salt–X followed by AX), the distractor would not gain access to the processor, and full processing of the target will result in full habituation of its unique and common features (Salt and X). In the backward order (AX → Salt–X), the target stimulus will not gain access to the information processor, and low habituation of the Salt element should be detected (the X element, present in the first compound, should be subject to habituation). Our results showed the opposite pattern of results: the Salt element was more salient after forward than backward pre-exposure. Robertson and Garrud (1983) also predict an order effect when the target and the distractor are dissimilar: when a target is followed by a dissimilar distractor (Salt–X → AY) the distractor should displace the target from the processor and its elements (Salt and X) should retain their salience or effectiveness. In the backward arrangement (AY → Salt–X), the target would displace the distractor from the processor, and processing of the target will result in full habituation of its unique and common features (Salt and X). Experiment 1 revealed, however, an equally preserved salience of the unique element Salt in the forward and the backward arrangements. So no evidence could be found to support the Robertson and Garrud (1983) hypothesis. At this point, we decided to focus our attention on the only group in which the salience of the unique feature Salt was significantly reduced during the pre-exposure phase: the Backward-Similar condition in which the animals were exposed to AX immediately followed by Salt–X. Assuming the principles of Wagner’s SOP model, we hypothesized that the presence of X in the first compound should result in full activation of the representation of this event. However, after a short delay, this activation would decay into a less effective or marginal A2 state of activation that prevents further activation into A1 even if the stimulus is physically presented again. That being the case, the Salt element in the second compound could be expected to be fully processed (and habituated), given that the potentially competing common element X would be in a state of marginal activation. This hypothesis can successfully account for the results observed in Experiment 1 of the present study. Furthermore, one prediction that could be derived from that hypothesis was that presenting the Salt element by itself (either in the Forward-Dissimilar or the Backward-Dissimilar condition) should result in full processing of that stimulus equivalent to the processing in the Backward-Similar condition. Experiment 2 confirmed the accuracy of this prediction. This pattern of results extends and complements the existent literature on distractor effects. Kaye et al. (1988) suggested that the similarity between the target and the distractor could account for the absence of a distractor effect either when the animals were given forward (the target followed by the distractor) or backward (the distractor followed by the target) pre-exposure. In both cases, the habituation of the common element X should generalize from the distractor to the target at the time of test, counteracting any distractor effect due to interruption of processing. However, this view overlooked the possible changes in the salience or effectiveness of the unique features of the target and the distractor: at the time of test, the net response observed would be controlled by the common elements, hindering any effect attributable to the salience or effectiveness of the unique features. In our research, we have gone a step further by assessing the effect of the order of presentation of the target and the distractor upon the habituation of the unique feature of the target stimulus. The present experiments have shown
A.A. Artigas et al. / Behavioural Processes 90 (2012) 204–209
that serial exposure to similar stimuli protects the salience of the unique features of the compound presented first. Taken together, the Kaye et al.’s study and the present results suggest that two mechanisms modulate the distractor effects: a Wagner’s like mechanism that protects the salience of some features of the pre-exposed compound stimuli, and the generalization of habituation between stimuli sharing a significant proportion of common elements. To conclude, the learning mechanism characterized in the present experiments seems to be adequate to account for distractor effects; more generally, it informs about the way in which similar stimuli presented closely in time are processed. References Artigas, A.A., Sansa, J., Blair, C.A.J., Hall, G., Prados, J., 2006. Enhanced discrimination between flavor stimuli: roles of salience modulation and inhibition. Journal of Experimental Psychology: Animal Behavior Processes 32, 173–177. Atkinson, R.C., Shiffrin, R.M., 1968. Human memory: a proposed system and its control processes. In: Spence, K.W., Spence, J.T. (Eds.), The Psychology of Learning and Motivation (vol. 2). Academic Press, New York, pp. 89–195. Dwyer, D.M., Bennett, C.H., Mackintosh, N.J., 2001. Evidence for inhibitory associations between the unique elements of two compound flavours. Quarterly Journal of Experimental Psychology 54B, 97–107. Dwyer, D.M., Mackintosh, N.J., 2002. Alternating exposure to two compound flavors creates inhibitory associations between their unique features. Animal Learning and Behavior 30, 177–200.
209
Fudim, O.K., 1978. Sensory preconditioning of flavors with a formalin-produced sodium need. Journal of Experimental Psychology: Animal Behavior Processes 4, 276–285. Green, K.F., Parker, L.A., 1975. Gustatory memory: incubation and interference. Behavioral Biology 13, 359–367. Kaye, H., Swietalski, N., Mackintosh, N.J., 1988. Habituation as a function of similarity and temporal location of target and distractor stimuli. Animal Learning & Behavior 16, 93–99. Rankin, C.H., Abrams, T., Barry, R.J., Bhatnagar, S., Clayton, D.F., Colombo, J., Coppola, G., Geyer, M.A., Glanzman, D.L., Marsland, S., Mcsweeney, F.K., Wilson, D.A., Wu, C., Thompson, R.F., 2009. Habituation revisited: an updated and revised description of the behavioural characteristics of habituation. Neurobiology of Learning and Memory 92, 135–138. Robertson, D., Garrud, P., 1983. Variable processing of flavours in rat STM. Animal Learning & Behavior 11, 474–482. Shanks, D.R., Preston, G.C., Stanhope, K.J., 1986. Effects of distractor familiarity on habituation of neophobia. Animal Learning & Behavior 14, 393–397. Symonds, M., Hall, G., Bailey, G.K., 2002. Perceptual learning with a sodium depletion procedure. Journal of Experimental Psychology: Animal Behavior Processes 28, 190–199. Thompson, R.F., Spencer, W.A., 1966. Habituation: a model phenomenon for the study of neuronal substrates of behaviour. Psychological Review 173, 16–43. Wagner, A.R., 1976. Priming in STM: an information-processing mechanism for self-generated or retrieval-generated depression in performance. In: Tighe, T.J., Leaton, R.N. (Eds.), Habituation: Perspectives From Child Development, Animal Behavior, and Neuropsychology. Lawrence Erlbaum Associates, Inc., Hillsdale, NJ, pp. 95–128. Wagner, A.R., 1981. SOP: a model of automatic memory processing in animal behavior. In: Spear, N.E., Miller, R.R. (Eds.), Information Processing in Animals: Memory Mechanisms. Lawrence Erlbaum Associates, Inc., Hillsdale, NJ, pp. 5–47.