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Age-dependent contextual effects on short-term active avoidance retention in rats
BEHAVIORAL AND NEURAL BIOLOGY 30, 250--259 (1980)
Age-Dependent Contextual Effects on Short-Term Active Avoidance Retention in Rats GAYLE S. SOLHEIM, JULIE G . HENSLER, AND NORMAN E . SPEAR 1
State University of New York at Binghamton Two experiments examined age-related differences in short-term retention of active avoidance in rats through manipulation of context. While adult and preweanling rats showed equally good immediate retention of the avoidance task when an odor contextual cue was held constant between training and testing, the performance of preweanlings was significantly disrupted compared to that of adults when the testing-context odor differed from that of training. The same results were obtained whether the animals had no prior experience with the odors (Experiment I) or had previously been exposed to the contextual cues (Experiment II). Results are considered in terms of their implications for the ontogeny of memory storage and retention.
The phenomenon of infantile amnesia, wherein immature animals show an exaggerated rate of forgetting over a long interval compared to mature animals, has been well documented (cf. Campbell & Spear, 1972; Campbell & Coulter, 1976). This differential forgetting has been shown to occur when acquisition rate is equivalent between infants and adults (cf. Feigley & Spear, 1970; Smith, 1968), and even when immature animals are overtrained on a task relative to the adults (Nagy & Mueller, 1973). Experimental investigations into the possible causes of this phenomenon have focused on a variety of factors, including neurophysiological growth between learning and testing (Campbell, Misanin, White, & Lytle, 1974), increased susceptibility to interference on the part of immature animals (Smith, 1978), and special characteristics of memory storage in younger organisms (Coulter, 1979; Gordon, 1979; Spear, 1979). While some support has been generated for each of these alternatives, Spear 1 This article was supported by grants from the National Science Foundation (BNS 74-24194 and BNS 78-02360) to the third author. The technical assistance of Norman G. Richter is gratefully acknowledged. Requests for reprints should be addressed to Dr. Spear, Department of Psychology, State University of New York at Binghamton, Binghamton, N.Y. 13901. 250 0163-1047/80/110250-10502.00/0 Copyright© 1980by AcademicPress, Inc. All rightsof reproductionin any form reserved.
AGE-DEPENDENTCONTEXTUALEFFECTS
251
(1979) has suggested several current circumstances that promote special interest in investigations relating to the last alternative. Differential memory storage during development may occur because immature animals either store fewer attributes of a given learning episode than do adults, or they store as many (or more) attributes but they store the " w r o n g " ones. Since various attributes of a memory may be differentially susceptible to sources of forgetting, immature animals could be attending to and storing attributes that are sufficient to promote learning and short-term retention but inadequate to support long-term retention. The younger animals, for example, may be processing and storing irrelevant redundant stimuli, such as extra-task contextual cues, at the expense of more predictive stimuli that would aid in later retention. Two sets of experiments recently have indicated profound effects of contextual features on learning, effects that were specific to immature animals. In both cases, the contextual features were some aspect of the animals' home environment. Smith and Spear (1978) found that the presence of home litter shavings significantly improved passive avoidance learning and increased spontaneous alternation in 16-day-old rat pups, an effect not found if clean shavings were used. Somewhat paradoxically, Infurna, Steinert, and Spear (1979) demonstrated that acquisition of a taste aversion was retarded in preweanling rats if illness was induced in the animals' home cage, but not if they were conditioned in a novel environment (for a similar result, see Martin & Alberts, 1979). In both series of experiments, learning on the part of adult rats was unaffected by these contextual features. Why home environmental stimuli should facilitate learning in one situation and disrupt it in another remains to be explained, but taken together, the above studies show an important influence of contextual events on acquisition and retention in immature animals, even when these events hold no obvious informational value to the animals about the task at hand. However, the contextual stimuli employed in these experiments have all been objects associated with the animals' home nests, stimuli that can be assumed to be of special significance to immature organisms which have spent their entire lives in that environment. Would younger animals be similarly affected by a contextual cue they were not so familiar with? If immature animals are processing more irrelevant stimuli than adults, then they should display impaired acquisition and/or retention when a task involves contextual cues other than those associated with home environments. EXPERIMENT I The first experiment was designed to assess the influence of a contextual change on the acquisition and short-term retention of active avoidance. Either lemon or peppermint odors were used as extra-task
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contextual stimuli during training. It was predicted that should younger animals store more irrelevant cues, changing the contextual odor cue from training to testing would significantly disrupt retention performance in preweanling rats relative to that of adults or of animals of either age when context was kept constant.
Method Subjects. The subjects were 32 female preweanling (20 days old) and 24 female adult (60-70 days old) Sprague-Dawley-derived albino rats bred and raised in the colony at the State University of New York at Binghamton. Preweanlings were kept with their parents and siblings in standard plastic maternity cages. Litter sizes ranged from 8 to 10 pups, with four females being used from each litter. Adult rats were housed in pairs in standard rodent cages. Food and water were available ad lib to all subjects. Apparatus. Training for the experimental subjects and testing for all subjects were conducted in a one-way avoidance apparatus, previously described by Klein and Spear (1969), with one white and one black chamber. A door separating the chambers could be lowered leaving a 2-cm hurdle between the chambers and simultaneously activating an intermittent tone (86 db) located beneath the center of the apparatus. A 1-mA scrambled footshock, provided by a Grason-Stadler shock generator, could be delivered through the grid floor of the white compartment. Both tone and shock were terminated by raising the door. Clear Plexiglas trays with odor-soaked cotton were fitted under the grids on both sides of the apparatus, and a wire mesh insert was placed over the grids on the black side. A 40-cm 3 smoked Plexiglas chamber with a grid floor served as the "training" apparatus for noncontingent footshock animals. The tone and shock sources were the same as for the avoidance apparatus. A large Plexiglas tray was fitted beneath the chamber for delivery of odors. Procedure. Subjects of each age were randomly assigned to groups, according to whether they were to receive active avoidance (AA) training or noncontingent footshock (NCFS), and whether the odor context cue during test was to be the same as, or different from, that of training. Acquisition trials for the AA animals were initiated by placing the subject on the white side of the avoidance apparatus, facing away from the door. Five seconds later, the door was dropped and the tone was activated. If the subject failed to cross (i.e., avoid) to the opposite side within 5 sec, the shock was administered. As soon as the rat crossed into the black chamber, the door was raised, terminating both tone and shock, and crossover latency was recorded. After each escape or avoidance, the animal was left on the black side for 10 sec before being removed to a holding cage for a 30-sec intertrial interval. Training continued until a
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criterion of three successive avoidances (latency less than 5 sec) was reached. Subjects who failed to reach the 3/3 criterion within 25 trials were eliminated. Three adults and two weanlings were discarded in this fashion. For each rat trained on AA, another of the same age was " y o k e d " by placing it in the N C F S chamber and matching number of trials and amount of tone, shock, and odor exposure on each trial to that of its AA counterpart. N C F S animals could not escape or avoid, but were removed to the holding cage for 30 sec after each trial and were otherwise treated exactly as those given avoidance training. During AA sessions, Plexiglas trays containing cotton soaked with 2 cc of McCormick extract (lemon or peppermint) were placed under each side of the apparatus just under the grid floors. Both trays contained the same odor. The same trays were fitted under the N C F S chamber for " y o k e d " N C F S animals. Half the animals in each of the eight groups were trained over one of the odors and half over the other. Immediately following the AA or N C F S session, each animal received 12 nonshock test trials in the white-black avoidance apparatus, with testing conducted over the same odor as that of training for half the subjects in each age group, while the odor was changed for the other half. Test trials included six active avoidance trials (animals started from the white side) interspersed among six passive avoidance trials (animals started from the black side), with trial sequence randomly determined. L a t e n c y to cross from one compartment to the other was recorded on each trial, with a maximum latency of 30 sec on each trial. Results and Discussion
An unequal-n's analysis of variance (ANOVA) applied to original learning scores revealed no differences between preweanlings and adults on number of trials to criterion, nor did training odor differentially affect acquisition within groups (both F ' s < 1). There were, however, significant performance differences as a function of contextual manipulations on test. A three-way (age x avoidance contingency x test odor) A N O V A analyzing white to black latencies on test trials showed a significant disruption of the acquired avoidance on the part of the preweanlings with the changed odor, reflected in the three-way interaction, F(I, 48) = 14.51,p < .001 (see Fig. 1). Significant main effects were also found for training condition and for age. Animals given only noncontingent shocks and no avoidance training crossed from white to black more slowly than trained animals, F(I, 48) = 28.74, p < .001. Preweanlings also had, overall, significantly longer crossover latencies than adults, F(l, 48) = 44.55,p < .001, but as can be seen in the open bars in Fig. l, this difference occurred only among preweanling N C F S animals
254
SOLHEIM, HENSLER, AND SPEAR ACTIVE AVOIDANCE
I J-"l WHITE TO BLACK [~
NCFS
BLACK TO WHITE
Ix
SAME DIFF SAME DIFF 20 DAY O L D S ADULTS
SAME DIFF 20 DAY OLDS
SAME DIFF ADULTS
AGE AND TEST ODOR
F[o. 1. Mean discriminative crossover latencies for preweanlings and adults in Experiment I as a function of training condition and odor present on nonshock test trials (same or different from that of training).
and AA preweanlings with changed odor, not a m o n g preweanlings with same odor on test as in training. The A N O V A on black to white latencies (shaded bars in Fig. 1) yielded a significant age x avoidance contingency interaction, F(1, 48) = 12.91, p < .001. While adults crossed more rapidly than preweanlings, this age difference was only found a m o n g animals given noncontingent footshock, not in avoidance-trained animals. There was also a significant age x test odor interaction, F(1,48) = 4.22, p < .05; the two adult groups tested o v e r an odor different than that of training crossed o v e r faster than adults tested o v e r the same odor, but for infants this difference did not occur. In s u m m a r y , the results of the first experiment indicate that the preweanlings' short-term retention of active avoidance was significantly disrupted by changing an irrelevant contextual cue. While not reflected in the white-to-black test trial latencies, there was some suggestion in blackto-white latencies that the adults with changed odor were also affected by the change. H o w e v e r , since the N C F S adults with a different test odor also crossed more rapidly from black to white than N C F S adults with the same odor, the observed difference in avoidance-trained adults is difficult to interpret. T h e r e was a possibility that the presence of the wire mesh insert on the black side influenced the p e r f o r m a n c e of the N C F S adults, w h e r e b y animals shocked on a grid floor preferred the wire mesh flooring when the same odor was present but showed no such preference w h e n tested in the presence of a different odor. This was assessed in the next experiment.
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E X P E R I M E N T II
While it seems clear from the first experiment that preweanlings are more susceptible than adults to disruption from a contextual change, it may be that a change to any unfamiliar stimulus during the test phase would have a disruptive effect due to novelty, though it is still interesting that only the preweanlings were affected by the change. Therefore it was the purpose of the second experiment to alleviate potential novelty effects by prefamiliarizing the animals with the odors to be used in training and testing. The wire mesh insert was also removed from the black side to avoid the possible difficulty with Experiment I.
Method Subjects. Subjects were 32 female preweanling (20 days old) and 24 female adult (60-70 days old) Sprague-Dawley-derived rats from the colony at SUNY Binghamton. Housing and feeding conditions were the same as in Experiment I. Apparatus. For odor preexposure, two standard metal rodent cages with slip-on tops and bottoms were used, modified by enclosing the wire mesh fronts with clear Plexiglas. A small Plexiglas box with one side open to the wire mesh of the carrying cage was attached to an opening cut in the center of the Plexiglas covers. This box held cotton to be soaked with odors. Training and testing apparatus were identical to those of the first experiment. Procedure. The experimental procedure was the same as for Experiment I with the addition of the preexposure sessions. During 2 days prior to training, all subjects received 20 min of preexposure to the odors to be used as contextual cues. On each day, the animals were placed in enclosed holding cages containing a piece of cotton soaked with 2 cc of either lemon or peppermint extract. Subjects received 10 min of exposure to each odor on each day, counterbalanced across days, with a 10-rain interval spent in the home cage between odors. Training and testing were conducted 24 hr after the second day of preexposure. Results and Discussion All four trained groups reached the avoidance criterion in about the same number of trials as in the previous experiment, and there were no differences between groups in trials to criterion, nor within-group differences due to training odor (both F's < l). Latency differences during the test as a function of contextual manipulations were again significant. A three-way (age x avoidance contingency x test odor) ANOVA on white to black latencies yielded a three-way interaction, F(1, 48) = 9.89, p < .01, in which AA preweanlings with changed odor slowed significantly on test trials compared to AA preweanlings with unchanged odor, while performance of adults and NCFS
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animals was not differentially affected (see Fig. 2). Significant main effects were found for avoidance contingency and for age; N C F S animals crossed more slowly than AA animals, F(1, 48) = 38.98, p < .001, and preweanlings were generally slower than adults, F(1, 48) = 35.13, p < .001. This latter effect, as can be seen in the open bars in Fig. 2 is again due to N C F S preweanlings and AA preweanlings with changed odor on test. AA preweanlings with same odor during training and testing crossed as rapidly as AA adults. Analysis of black-to-white latencies yielded a significant age × avoidance contingency interaction, F(1, 48) = 11.65, p < .001. While adults c r o s s e d more rapidly than preweanlings, this age difference was reflected only among the noncontingent shock animals and not among the avoidance-trained animals. The results of Experiment II replicated those of Experiment I. Even with previous exposure to the odors, changing the irrelevant contextual cue from training to testing disrupted the retention performance of preweanlings but not that of adults. An interesting Jifference between the two experiments is that by removing the wire mesh from the black side, the N C F S adults in the second experiment no longer demonstrated any side preference. GENERAL
DISCUSSION
The results from these two experiments, unlike those of Infurna et al. (1979) and Smith and Spear (1978), showed no differential effects of an extra-task contextual cue on acquisition of the task. Both age groups
3~
ACTIVEAVOIDANCE
I i'-'] WHITE TO BLACK l [ ] BLACK TO WHITE
NCFS
2
>- 2
=o uJ J
,.=,
I
o Ix
SAME D1FF S A M E DIFF SAME DIFF SAME DIFF 20 DAY OLDS ADULTS 20 DAY O L D S ADULTS AGE AND TEST ODOR
FIG. 2. Mean discriminative crossover latencies for preweanlings and adults in Experiment [I as a function of training condition and odor present on nonshock test trials (same or different from that of training).
AGE-DEPENDENT CONTEXTUAL EFFECTS
257
reached the avoidance criterion in the same number of trials. Perhaps this was because the lemon and peppermint odors present during learning had no prior associative value for the animals, whereas odors from the home environment do. However, a task-irrelevant change in the contextual odor cue did significantly disrupt the short-term retention performance of preweanlings while leaving that of adults unchanged. These results support the suggestion that in comparison with adults, immature animals make use of different attributes in different degrees to represent the learning episode. They also extend the ontogenetic study of contextual influences from odors associated with the home environment to those that should be less familiar or meaningful to the animals. This differential use of redundant and irrelevant cues could account for some of the exaggerated long-term forgetting observed on the part of immature animals (i.e., infantile amnesia), especially through interaction with other sources of forgetting. Retention is often critically dependent on the degree to which the context of testing matches that of original learning (Spear, 1978, Chap. 2), and the typical experiment tries to keep the match exact. However, a contextual cue such as odor, especially when it is an extra-task stimulus, may be much less under the control of the experimenter than a tone or the color of the apparatus. This would make it less likely that the exact cue would be available for retrieval of a memory after a long interval. Alternatively, a memory stored primarily in terms of odor attributes could be especially susceptible to interference during the retention interval. Rats are obviously more apt to come into contact with other odors during the interval than with other tones, shocks, or black-white boxes, although it is unclear what implications this might have for age-related differences in forgetting. It should be mentioned that while we could predict that the younger rats' performance would be significantly disrupted by a contextual change relative to the performance of adults, we were somewhat surprised at the magnitude of the difference. This may be due to the relatively few trials (three) that were used to define criterion performance. It is possible that three trials were sufficient for the adults to develop an association between the avoidance cue and running to safety on the black side while learning that odor was irrelevant, whereas three trials were not enough for the infants to learn that odor was nonpredictive. Perhaps with overtraining the preweanlings' dependence on contextual cues could be lessened. Alternatively, it could be argued that detection of odors and therefore of the odor change was simply poorer among the adults. Results of other experiments suggest that this is an unlikely explanation. For example, Kessler and Spear (cited in Spear, 1979, but otherwise unpublished) gave both preweanlings and adults footshocks paired with lemon or peppermint
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odors and found avoidance of those odors 24 hr later to be equivalent between the two ages. One would not expect these results if adults were deficient in detecting the conditioning odors. Data concerning the ontogeny of odor detection, gathered recently by J. R. Alberts (personal communication, April 9, 1980), also suggest that age differences in odor detection alone could not account for the present results. It seems more likely that the adults were simply less attentive to irrelevant contextual features in our experiments than were the younger animals. In this current pair of experiments and others cited (Infurna et al., 1979; Smith & Spear, 1978), the contextual events used to demonstrate differential effects on immature and adult animals' performance can all be said to depend to some extent on odors (e.g., smell of siblings, home nest shavings, etc.). It remains to be seen how general the effect is for contextual events other than odors. Some indirect evidence suggests it may be very general. Brennan (1979) examined age-related differences in the extinction of two-way active avoidance in rats through manipulation of stimulus context. He found more pronounced disruption of extinction in preweanlings, compared to adults, when either a conspecific or a novel light were introduced into one end of the apparatus during extinction trials. REFERENCES Brennan, J. F. (1979). Differential extinction of two-way active avoidance in young and adult rats. Developmental Psychobiology, 12, 27-37. Campbell, B. A., & Coulter, X. (1976). Ontogeny of learning and memory. In M. R. Rosenzweig & E. L. Bennett (Eds.), Neuromechanisms of Learning and Memory. Cambridge, Mass.: MIT Press. Campbell, B. A., & Spear, N. E. (1972). Ontogeny of memory. Psychological Review, 79, 215-236. Campbell, B. A., Misanin, J. R., White, B. C., & Lytle, L. D. (1974). Species differences in ontogeny of memory: Indirect support for neural maturation as a determinant of forgetting. Journal of Comparative and Physiological Psychology, 87, 193-202. Coulter, X. (1979). The determinants of infantile amnesia. In N. E. Spear & B. A. Campbell (Eds.), Ontogeny of Learning and Memory. Hillsdale, N.J.: Lawrence Erlbaum Associates. Feigley, D. A., & Spear, N. E. (1970). Effect of age and punishment condition on long-term retention by the rat of active- and passive-avoidance learning. Journal of Comparative and Physiological Psychology, 73, 515-526. Gordon, W. C. (1979). Age: Is it a constraint on memory content? In N. E. Spear & B. A. Campbell (Eds.), Ontogeny of Learning and Memory. Hillsdale, N.J.: Lawrence Erlbaum Associates. Infurna, R. N., Steinert, P. A., & Spear, N. E. (1979). Ontogenetic changes in the modulation of taste aversion learning by home environmental cues in rats. Journal of Comparative and Physiological Psychology, 93, 1097-1108. Klein, S. B., & Spear, N. E. Influence of age on short-term retention of active avoidance learning in rats. Journal of Comparative and Physiological Psychology, 1969, 69, 583-589.
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Martin, L. T., & Alberts, J. R. (1979). Taste aversions to mother's milk: The age-related role of nursing in acquisition and expression of a learned association. Journal of Comparative and Physiological Psychology, 93, 430-445. Nagy, Z. M., & Mueller, P. M. (1973). Effects of amount of original training upon onset of a 24-hour memory capacity in neonatal mice. Journal of Comparative and Physiological Psychology, 85, 151-159. Smith, G. J. (1978). A developmental study of the effects of noncontingent and contingent learning experience on subsequent learning and retention of a discrimination response. Unpublished M.A. Thesis, SUNY Binghamton. Smith, G. J., & Spear, N. E. (1978). Effects of the home environment on withholding behaviors and conditioning in infant and neonatal rats. Science, 202, 327-329. Smith, N. (1968). Effects of interpolated learning on the retention of an escape response in rats as a function of age. Journal of Comparative and Physiological Psychology, 65, 422-426. Spear, N. E. (1978). The Processing of Memories: Forgetting and Retention. Hillsdale, N.J.: Lawrence Erlbaum Associates. Spear, N. E. (1979). Memory storage factors leading to infantile amnesia. In G. H. Bower (Ed.), The Psychology of Learning and Motivation, Vol. 13. New York: Academic Press.
Age-Dependent Contextual Effects on Short-Term Active Avoidance Retention in Rats GAYLE S. SOLHEIM, JULIE G . HENSLER, AND NORMAN E . SPEAR 1
State University of New York at Binghamton Two experiments examined age-related differences in short-term retention of active avoidance in rats through manipulation of context. While adult and preweanling rats showed equally good immediate retention of the avoidance task when an odor contextual cue was held constant between training and testing, the performance of preweanlings was significantly disrupted compared to that of adults when the testing-context odor differed from that of training. The same results were obtained whether the animals had no prior experience with the odors (Experiment I) or had previously been exposed to the contextual cues (Experiment II). Results are considered in terms of their implications for the ontogeny of memory storage and retention.
The phenomenon of infantile amnesia, wherein immature animals show an exaggerated rate of forgetting over a long interval compared to mature animals, has been well documented (cf. Campbell & Spear, 1972; Campbell & Coulter, 1976). This differential forgetting has been shown to occur when acquisition rate is equivalent between infants and adults (cf. Feigley & Spear, 1970; Smith, 1968), and even when immature animals are overtrained on a task relative to the adults (Nagy & Mueller, 1973). Experimental investigations into the possible causes of this phenomenon have focused on a variety of factors, including neurophysiological growth between learning and testing (Campbell, Misanin, White, & Lytle, 1974), increased susceptibility to interference on the part of immature animals (Smith, 1978), and special characteristics of memory storage in younger organisms (Coulter, 1979; Gordon, 1979; Spear, 1979). While some support has been generated for each of these alternatives, Spear 1 This article was supported by grants from the National Science Foundation (BNS 74-24194 and BNS 78-02360) to the third author. The technical assistance of Norman G. Richter is gratefully acknowledged. Requests for reprints should be addressed to Dr. Spear, Department of Psychology, State University of New York at Binghamton, Binghamton, N.Y. 13901. 250 0163-1047/80/110250-10502.00/0 Copyright© 1980by AcademicPress, Inc. All rightsof reproductionin any form reserved.
AGE-DEPENDENTCONTEXTUALEFFECTS
251
(1979) has suggested several current circumstances that promote special interest in investigations relating to the last alternative. Differential memory storage during development may occur because immature animals either store fewer attributes of a given learning episode than do adults, or they store as many (or more) attributes but they store the " w r o n g " ones. Since various attributes of a memory may be differentially susceptible to sources of forgetting, immature animals could be attending to and storing attributes that are sufficient to promote learning and short-term retention but inadequate to support long-term retention. The younger animals, for example, may be processing and storing irrelevant redundant stimuli, such as extra-task contextual cues, at the expense of more predictive stimuli that would aid in later retention. Two sets of experiments recently have indicated profound effects of contextual features on learning, effects that were specific to immature animals. In both cases, the contextual features were some aspect of the animals' home environment. Smith and Spear (1978) found that the presence of home litter shavings significantly improved passive avoidance learning and increased spontaneous alternation in 16-day-old rat pups, an effect not found if clean shavings were used. Somewhat paradoxically, Infurna, Steinert, and Spear (1979) demonstrated that acquisition of a taste aversion was retarded in preweanling rats if illness was induced in the animals' home cage, but not if they were conditioned in a novel environment (for a similar result, see Martin & Alberts, 1979). In both series of experiments, learning on the part of adult rats was unaffected by these contextual features. Why home environmental stimuli should facilitate learning in one situation and disrupt it in another remains to be explained, but taken together, the above studies show an important influence of contextual events on acquisition and retention in immature animals, even when these events hold no obvious informational value to the animals about the task at hand. However, the contextual stimuli employed in these experiments have all been objects associated with the animals' home nests, stimuli that can be assumed to be of special significance to immature organisms which have spent their entire lives in that environment. Would younger animals be similarly affected by a contextual cue they were not so familiar with? If immature animals are processing more irrelevant stimuli than adults, then they should display impaired acquisition and/or retention when a task involves contextual cues other than those associated with home environments. EXPERIMENT I The first experiment was designed to assess the influence of a contextual change on the acquisition and short-term retention of active avoidance. Either lemon or peppermint odors were used as extra-task
252
SOLHEIM, HENSLER, AND SPEAR
contextual stimuli during training. It was predicted that should younger animals store more irrelevant cues, changing the contextual odor cue from training to testing would significantly disrupt retention performance in preweanling rats relative to that of adults or of animals of either age when context was kept constant.
Method Subjects. The subjects were 32 female preweanling (20 days old) and 24 female adult (60-70 days old) Sprague-Dawley-derived albino rats bred and raised in the colony at the State University of New York at Binghamton. Preweanlings were kept with their parents and siblings in standard plastic maternity cages. Litter sizes ranged from 8 to 10 pups, with four females being used from each litter. Adult rats were housed in pairs in standard rodent cages. Food and water were available ad lib to all subjects. Apparatus. Training for the experimental subjects and testing for all subjects were conducted in a one-way avoidance apparatus, previously described by Klein and Spear (1969), with one white and one black chamber. A door separating the chambers could be lowered leaving a 2-cm hurdle between the chambers and simultaneously activating an intermittent tone (86 db) located beneath the center of the apparatus. A 1-mA scrambled footshock, provided by a Grason-Stadler shock generator, could be delivered through the grid floor of the white compartment. Both tone and shock were terminated by raising the door. Clear Plexiglas trays with odor-soaked cotton were fitted under the grids on both sides of the apparatus, and a wire mesh insert was placed over the grids on the black side. A 40-cm 3 smoked Plexiglas chamber with a grid floor served as the "training" apparatus for noncontingent footshock animals. The tone and shock sources were the same as for the avoidance apparatus. A large Plexiglas tray was fitted beneath the chamber for delivery of odors. Procedure. Subjects of each age were randomly assigned to groups, according to whether they were to receive active avoidance (AA) training or noncontingent footshock (NCFS), and whether the odor context cue during test was to be the same as, or different from, that of training. Acquisition trials for the AA animals were initiated by placing the subject on the white side of the avoidance apparatus, facing away from the door. Five seconds later, the door was dropped and the tone was activated. If the subject failed to cross (i.e., avoid) to the opposite side within 5 sec, the shock was administered. As soon as the rat crossed into the black chamber, the door was raised, terminating both tone and shock, and crossover latency was recorded. After each escape or avoidance, the animal was left on the black side for 10 sec before being removed to a holding cage for a 30-sec intertrial interval. Training continued until a
AGE-DEPENDENT CONTEXTUAL EFFECTS
253
criterion of three successive avoidances (latency less than 5 sec) was reached. Subjects who failed to reach the 3/3 criterion within 25 trials were eliminated. Three adults and two weanlings were discarded in this fashion. For each rat trained on AA, another of the same age was " y o k e d " by placing it in the N C F S chamber and matching number of trials and amount of tone, shock, and odor exposure on each trial to that of its AA counterpart. N C F S animals could not escape or avoid, but were removed to the holding cage for 30 sec after each trial and were otherwise treated exactly as those given avoidance training. During AA sessions, Plexiglas trays containing cotton soaked with 2 cc of McCormick extract (lemon or peppermint) were placed under each side of the apparatus just under the grid floors. Both trays contained the same odor. The same trays were fitted under the N C F S chamber for " y o k e d " N C F S animals. Half the animals in each of the eight groups were trained over one of the odors and half over the other. Immediately following the AA or N C F S session, each animal received 12 nonshock test trials in the white-black avoidance apparatus, with testing conducted over the same odor as that of training for half the subjects in each age group, while the odor was changed for the other half. Test trials included six active avoidance trials (animals started from the white side) interspersed among six passive avoidance trials (animals started from the black side), with trial sequence randomly determined. L a t e n c y to cross from one compartment to the other was recorded on each trial, with a maximum latency of 30 sec on each trial. Results and Discussion
An unequal-n's analysis of variance (ANOVA) applied to original learning scores revealed no differences between preweanlings and adults on number of trials to criterion, nor did training odor differentially affect acquisition within groups (both F ' s < 1). There were, however, significant performance differences as a function of contextual manipulations on test. A three-way (age x avoidance contingency x test odor) A N O V A analyzing white to black latencies on test trials showed a significant disruption of the acquired avoidance on the part of the preweanlings with the changed odor, reflected in the three-way interaction, F(I, 48) = 14.51,p < .001 (see Fig. 1). Significant main effects were also found for training condition and for age. Animals given only noncontingent shocks and no avoidance training crossed from white to black more slowly than trained animals, F(I, 48) = 28.74, p < .001. Preweanlings also had, overall, significantly longer crossover latencies than adults, F(l, 48) = 44.55,p < .001, but as can be seen in the open bars in Fig. l, this difference occurred only among preweanling N C F S animals
254
SOLHEIM, HENSLER, AND SPEAR ACTIVE AVOIDANCE
I J-"l WHITE TO BLACK [~
NCFS
BLACK TO WHITE
Ix
SAME DIFF SAME DIFF 20 DAY O L D S ADULTS
SAME DIFF 20 DAY OLDS
SAME DIFF ADULTS
AGE AND TEST ODOR
F[o. 1. Mean discriminative crossover latencies for preweanlings and adults in Experiment I as a function of training condition and odor present on nonshock test trials (same or different from that of training).
and AA preweanlings with changed odor, not a m o n g preweanlings with same odor on test as in training. The A N O V A on black to white latencies (shaded bars in Fig. 1) yielded a significant age x avoidance contingency interaction, F(1, 48) = 12.91, p < .001. While adults crossed more rapidly than preweanlings, this age difference was only found a m o n g animals given noncontingent footshock, not in avoidance-trained animals. There was also a significant age x test odor interaction, F(1,48) = 4.22, p < .05; the two adult groups tested o v e r an odor different than that of training crossed o v e r faster than adults tested o v e r the same odor, but for infants this difference did not occur. In s u m m a r y , the results of the first experiment indicate that the preweanlings' short-term retention of active avoidance was significantly disrupted by changing an irrelevant contextual cue. While not reflected in the white-to-black test trial latencies, there was some suggestion in blackto-white latencies that the adults with changed odor were also affected by the change. H o w e v e r , since the N C F S adults with a different test odor also crossed more rapidly from black to white than N C F S adults with the same odor, the observed difference in avoidance-trained adults is difficult to interpret. T h e r e was a possibility that the presence of the wire mesh insert on the black side influenced the p e r f o r m a n c e of the N C F S adults, w h e r e b y animals shocked on a grid floor preferred the wire mesh flooring when the same odor was present but showed no such preference w h e n tested in the presence of a different odor. This was assessed in the next experiment.
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E X P E R I M E N T II
While it seems clear from the first experiment that preweanlings are more susceptible than adults to disruption from a contextual change, it may be that a change to any unfamiliar stimulus during the test phase would have a disruptive effect due to novelty, though it is still interesting that only the preweanlings were affected by the change. Therefore it was the purpose of the second experiment to alleviate potential novelty effects by prefamiliarizing the animals with the odors to be used in training and testing. The wire mesh insert was also removed from the black side to avoid the possible difficulty with Experiment I.
Method Subjects. Subjects were 32 female preweanling (20 days old) and 24 female adult (60-70 days old) Sprague-Dawley-derived rats from the colony at SUNY Binghamton. Housing and feeding conditions were the same as in Experiment I. Apparatus. For odor preexposure, two standard metal rodent cages with slip-on tops and bottoms were used, modified by enclosing the wire mesh fronts with clear Plexiglas. A small Plexiglas box with one side open to the wire mesh of the carrying cage was attached to an opening cut in the center of the Plexiglas covers. This box held cotton to be soaked with odors. Training and testing apparatus were identical to those of the first experiment. Procedure. The experimental procedure was the same as for Experiment I with the addition of the preexposure sessions. During 2 days prior to training, all subjects received 20 min of preexposure to the odors to be used as contextual cues. On each day, the animals were placed in enclosed holding cages containing a piece of cotton soaked with 2 cc of either lemon or peppermint extract. Subjects received 10 min of exposure to each odor on each day, counterbalanced across days, with a 10-rain interval spent in the home cage between odors. Training and testing were conducted 24 hr after the second day of preexposure. Results and Discussion All four trained groups reached the avoidance criterion in about the same number of trials as in the previous experiment, and there were no differences between groups in trials to criterion, nor within-group differences due to training odor (both F's < l). Latency differences during the test as a function of contextual manipulations were again significant. A three-way (age x avoidance contingency x test odor) ANOVA on white to black latencies yielded a three-way interaction, F(1, 48) = 9.89, p < .01, in which AA preweanlings with changed odor slowed significantly on test trials compared to AA preweanlings with unchanged odor, while performance of adults and NCFS
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animals was not differentially affected (see Fig. 2). Significant main effects were found for avoidance contingency and for age; N C F S animals crossed more slowly than AA animals, F(1, 48) = 38.98, p < .001, and preweanlings were generally slower than adults, F(1, 48) = 35.13, p < .001. This latter effect, as can be seen in the open bars in Fig. 2 is again due to N C F S preweanlings and AA preweanlings with changed odor on test. AA preweanlings with same odor during training and testing crossed as rapidly as AA adults. Analysis of black-to-white latencies yielded a significant age × avoidance contingency interaction, F(1, 48) = 11.65, p < .001. While adults c r o s s e d more rapidly than preweanlings, this age difference was reflected only among the noncontingent shock animals and not among the avoidance-trained animals. The results of Experiment II replicated those of Experiment I. Even with previous exposure to the odors, changing the irrelevant contextual cue from training to testing disrupted the retention performance of preweanlings but not that of adults. An interesting Jifference between the two experiments is that by removing the wire mesh from the black side, the N C F S adults in the second experiment no longer demonstrated any side preference. GENERAL
DISCUSSION
The results from these two experiments, unlike those of Infurna et al. (1979) and Smith and Spear (1978), showed no differential effects of an extra-task contextual cue on acquisition of the task. Both age groups
3~
ACTIVEAVOIDANCE
I i'-'] WHITE TO BLACK l [ ] BLACK TO WHITE
NCFS
2
>- 2
=o uJ J
,.=,
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o Ix
SAME D1FF S A M E DIFF SAME DIFF SAME DIFF 20 DAY OLDS ADULTS 20 DAY O L D S ADULTS AGE AND TEST ODOR
FIG. 2. Mean discriminative crossover latencies for preweanlings and adults in Experiment [I as a function of training condition and odor present on nonshock test trials (same or different from that of training).
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reached the avoidance criterion in the same number of trials. Perhaps this was because the lemon and peppermint odors present during learning had no prior associative value for the animals, whereas odors from the home environment do. However, a task-irrelevant change in the contextual odor cue did significantly disrupt the short-term retention performance of preweanlings while leaving that of adults unchanged. These results support the suggestion that in comparison with adults, immature animals make use of different attributes in different degrees to represent the learning episode. They also extend the ontogenetic study of contextual influences from odors associated with the home environment to those that should be less familiar or meaningful to the animals. This differential use of redundant and irrelevant cues could account for some of the exaggerated long-term forgetting observed on the part of immature animals (i.e., infantile amnesia), especially through interaction with other sources of forgetting. Retention is often critically dependent on the degree to which the context of testing matches that of original learning (Spear, 1978, Chap. 2), and the typical experiment tries to keep the match exact. However, a contextual cue such as odor, especially when it is an extra-task stimulus, may be much less under the control of the experimenter than a tone or the color of the apparatus. This would make it less likely that the exact cue would be available for retrieval of a memory after a long interval. Alternatively, a memory stored primarily in terms of odor attributes could be especially susceptible to interference during the retention interval. Rats are obviously more apt to come into contact with other odors during the interval than with other tones, shocks, or black-white boxes, although it is unclear what implications this might have for age-related differences in forgetting. It should be mentioned that while we could predict that the younger rats' performance would be significantly disrupted by a contextual change relative to the performance of adults, we were somewhat surprised at the magnitude of the difference. This may be due to the relatively few trials (three) that were used to define criterion performance. It is possible that three trials were sufficient for the adults to develop an association between the avoidance cue and running to safety on the black side while learning that odor was irrelevant, whereas three trials were not enough for the infants to learn that odor was nonpredictive. Perhaps with overtraining the preweanlings' dependence on contextual cues could be lessened. Alternatively, it could be argued that detection of odors and therefore of the odor change was simply poorer among the adults. Results of other experiments suggest that this is an unlikely explanation. For example, Kessler and Spear (cited in Spear, 1979, but otherwise unpublished) gave both preweanlings and adults footshocks paired with lemon or peppermint
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odors and found avoidance of those odors 24 hr later to be equivalent between the two ages. One would not expect these results if adults were deficient in detecting the conditioning odors. Data concerning the ontogeny of odor detection, gathered recently by J. R. Alberts (personal communication, April 9, 1980), also suggest that age differences in odor detection alone could not account for the present results. It seems more likely that the adults were simply less attentive to irrelevant contextual features in our experiments than were the younger animals. In this current pair of experiments and others cited (Infurna et al., 1979; Smith & Spear, 1978), the contextual events used to demonstrate differential effects on immature and adult animals' performance can all be said to depend to some extent on odors (e.g., smell of siblings, home nest shavings, etc.). It remains to be seen how general the effect is for contextual events other than odors. Some indirect evidence suggests it may be very general. Brennan (1979) examined age-related differences in the extinction of two-way active avoidance in rats through manipulation of stimulus context. He found more pronounced disruption of extinction in preweanlings, compared to adults, when either a conspecific or a novel light were introduced into one end of the apparatus during extinction trials. REFERENCES Brennan, J. F. (1979). Differential extinction of two-way active avoidance in young and adult rats. Developmental Psychobiology, 12, 27-37. Campbell, B. A., & Coulter, X. (1976). Ontogeny of learning and memory. In M. R. Rosenzweig & E. L. Bennett (Eds.), Neuromechanisms of Learning and Memory. Cambridge, Mass.: MIT Press. Campbell, B. A., & Spear, N. E. (1972). Ontogeny of memory. Psychological Review, 79, 215-236. Campbell, B. A., Misanin, J. R., White, B. C., & Lytle, L. D. (1974). Species differences in ontogeny of memory: Indirect support for neural maturation as a determinant of forgetting. Journal of Comparative and Physiological Psychology, 87, 193-202. Coulter, X. (1979). The determinants of infantile amnesia. In N. E. Spear & B. A. Campbell (Eds.), Ontogeny of Learning and Memory. Hillsdale, N.J.: Lawrence Erlbaum Associates. Feigley, D. A., & Spear, N. E. (1970). Effect of age and punishment condition on long-term retention by the rat of active- and passive-avoidance learning. Journal of Comparative and Physiological Psychology, 73, 515-526. Gordon, W. C. (1979). Age: Is it a constraint on memory content? In N. E. Spear & B. A. Campbell (Eds.), Ontogeny of Learning and Memory. Hillsdale, N.J.: Lawrence Erlbaum Associates. Infurna, R. N., Steinert, P. A., & Spear, N. E. (1979). Ontogenetic changes in the modulation of taste aversion learning by home environmental cues in rats. Journal of Comparative and Physiological Psychology, 93, 1097-1108. Klein, S. B., & Spear, N. E. Influence of age on short-term retention of active avoidance learning in rats. Journal of Comparative and Physiological Psychology, 1969, 69, 583-589.
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Martin, L. T., & Alberts, J. R. (1979). Taste aversions to mother's milk: The age-related role of nursing in acquisition and expression of a learned association. Journal of Comparative and Physiological Psychology, 93, 430-445. Nagy, Z. M., & Mueller, P. M. (1973). Effects of amount of original training upon onset of a 24-hour memory capacity in neonatal mice. Journal of Comparative and Physiological Psychology, 85, 151-159. Smith, G. J. (1978). A developmental study of the effects of noncontingent and contingent learning experience on subsequent learning and retention of a discrimination response. Unpublished M.A. Thesis, SUNY Binghamton. Smith, G. J., & Spear, N. E. (1978). Effects of the home environment on withholding behaviors and conditioning in infant and neonatal rats. Science, 202, 327-329. Smith, N. (1968). Effects of interpolated learning on the retention of an escape response in rats as a function of age. Journal of Comparative and Physiological Psychology, 65, 422-426. Spear, N. E. (1978). The Processing of Memories: Forgetting and Retention. Hillsdale, N.J.: Lawrence Erlbaum Associates. Spear, N. E. (1979). Memory storage factors leading to infantile amnesia. In G. H. Bower (Ed.), The Psychology of Learning and Motivation, Vol. 13. New York: Academic Press.