contextual gating of memory retrieval

Contextual Gating of Memory Retrieval

JUDITH BUTLER

Department of Psychology Rutgers University

New Brunswick, New Jersey

CAROLYN ROVEE-COLLIER

In two experiments, 3-month-old infants learned to move a crib mobile (the cue) in the presence of a distinctive crib bumper (the context) by operant kicking. In Experiment lA, infants were trained for 2 days and tested either 1, 3, or 5 days later with one of four sameidifferent cueicontext combinations. After all delays, infants tested with the original cue and context exhibited excellent retention, and those tested with a different cue and context exhibited none. Changing the context but not the cue disrupted retention after 3 and 5 days but not after 1 day; in contrast, changing the cue but not the context disrupted retention after all delays. In Experiment lB, the failure of a contextual change to impair retention after 1 day was replicated. In Experiment 2 , three sameidifferent cueicontext combinations were used as reminders in a reactivation paradigm, and all infants were tested 1 day later with their original training combination. A change in either the context or the cue significantly impaired the effectiveness of the reminder. These results reveal not only that contextual information is incorporated into the memory representations of very immature infants but also that memory retrieval is highly specific to the context in which an event was originally encoded. This specificity buffers against generalized memory retrieval after long retention intervals. The data are consistent with Reeves and Sperling’s 1986 model of attention-gating. The context appears to serve as the initial gate for attention to potentially effective retrieval cues.

All behavior occurs in a context. No situation is context-free. Yet the effect of contextual cues on learning and memory in human infants has received little attention. Much of this neglect reflects the widely held belief that “virtually all learning during infancy is . . . independent of context” (Nadel, Willner, & Kurz, 1985, p. 398). This is based on the conclusion that the delayed maturation of the hippocampus precludes storage of representations of the environmental context in which an event occurs prior to the eighth or ninth postnatal month (Nadel & Zola- Morgan, 1984; Olson & Strauss, 1984; Schacter & Moscovitch, 1984). Support for this conclusion has been drawn from studies of infant visual recognition memory

Reprint requests should be sent to Carolyn Rovee-Collier, Department of Psychology, Busch Campus, Rutgers University, New Brunswick, NJ 08903, 0.S.A.

Received for publication 5 August 1988 Revised for publication 30 January 1989; 21 April 1989 Accepted at Wiley 10 May 1989

Developmental Psychobiology 22(6):533-552 ( 1989) 0 1989 by John Wiley & Sons, Inc. CCC 0012- 16301891060533-20$04.00

534 BUTLER AND ROVEE-COLLIER

(Olson & Sherman, 1983; Werner & Perlmutter, 1979), adult amnesic patients (Schacter & Moscovitch, 1984; Squire, Cohen, & Nadel, 1984), and lesioned animals (for review, see Nadel & Zola-Morgan, 1984). In addition, rat pups begin to use spatial landmarks at 20-21 days (Nadel et al., 1985; Nadel & Zola-Morgan, 1984; Rudy, Stadler-Morris, & Albert, 1987), when their hippocampal system first becomes functional, and human infants begin to do so at 8-9 months of age (Acredolo, 1978; Acredolo & Evans, 1980; Bremner, 1978; Cornell & Heth, 1979; Keating, McKenzie, & Day, 1986).

Recent evidence from studies of animal and human infants has challenged the assumption that younger organisms lack the capacity to encode, store, and use information about where learning occurs. Richardson, Riccio, and McKenney (1988) found that a newly acquired memory of immature rat pups was disrupted if the characteristics of the test room were altered 5 min after the conclusion of training. ,The reactivated memory of training was disrupted by the same contextual change 25-30 min after the presentation of the remainder. Similarly, Rovee- Collier, Griesler, and Earley (1985) found that retention of an operant contingency by 3-month-old human infants was disrupted if the physical setting of training was changed during testing a week later. Using the training context as the sole reminder, they also were able to reactivate the memory 2 weeks later. Because reinstatement is generally recognized as a context-dependent phenomenon (Bou- ton & Bolles, 1979; Nadel et al., 1985), the latter demonstration presents an additional problem for the maturational hypothesis. Either the hippocampus achieves functional maturity earlier than previously thought or some other memory system mediates the processing of contextual information early in development.

A number of different but not necessarily mutually exclusive accounts have been proposed for the effect of context on learning and retention (see Balsam, 1985). For instance, contextual stimuli may compete with the nominal stimulus (the CS or S + ) for associative strength (Rescorla & Wagner, 1972), may facilitate responding by acting as a retrieval cue for CS-US associations (Konorski, 1967; Spear, 1973), or may set the occasion for a particular contingency, much like a conditional discriminative stimulus (Holland, 1985). Although all accounts predict that a contextual change at the time of testing will disrupt performance, none predicts if or how the influence of the context changes over time. This question is of particular interest to students of early development because of the theoretical importance accorded contextual drift (Bower, 1967; Estes, 1950) and perceived changes in context by rapidly developing organisms as sources of infantile amnesia (Campbell & Spear, 1972).

Riccio, Richardson, and Ebner (1984) have proposed that contextual information is forgotten more rapidly than other attributes represented in the memory of an event and therefore is unlikely to affect retention after long delays. Their proposal was based on evidence that (1) the disrupting effect of a change in the context is greatest closest in time to original training, and that (2) performance in an altered test context actually improves as the retention interval increases until it ultimately is equivalent to performance in an unchanged context. If contextual change does not affect retention after shorter retention intervals, they argued, it is unlikely to do so after even longer delays.

CONTEXTUAL GATING 535

A response pattern identical to that described by Riccio et al. (1984) was obtained in a study with 3-month-old human infants (Rovee-Collier & Sullivan, 1980), but this pattern was produced by a change in the nominal cue (the S+), not by a contextual change. After a l-day retention interval, responding was com- pletely disrupted by a change in the visual characteristics of the test cue; as the retention interval increased, the disrupting effect of an altered cue progressively lessened until, after a retention interval of 3-4 days, performance was excellent whether the test cue was the same as or different from the training cue. In this study, however, all training and testing was in the familiar context of infants’ home cribs. In the study cited earlier (Rovee-Collier et al., 1985), when training was in a highly distinctive context, a change in that context significantly disrupted performance after a retention interval of 7 days even though the original cue was present during the test. Considered together, these findings raise the possibility that the cue and the physical context affect retention differently over time. Whether or how they might interact, however, is not known.

The present experiments with 3-month-olds were designed to examine the temporal course of contextual influences on retention and their relation to the nominal cue. Infants were trained to move an overhead crib mobile (the cue) in the presence of a distinctively colored and patterned crib liner (the context) by operant kicking. In the first study, they were tested with different cuekontext combinations (samehame, same/different, differenthame, different/different) after each of the three retention intervals (1, 3, 5 days) used by Rovee-Collier and Sullivan (1980). In the second study, the effectiveness of these combinations as retrieval cues after an even longer delay was assessed in a reactivation paradigm.

Experiment 1A

Method

Subjects Subjects were 72 infants (39 males, 33 females) with a mean age of 90.6 days

(SD = 9.2). Infants were recruited through use of published birth announcements and by word of mouth. Testing of additional infants was discontinued as a result of continuous crying for 2 min during any of the three sessions (n = 25), failure to meet the learning criterion (a response rate at least 1.5 times operant level in 2 of any 3 consecutive min during acquisition in sessions I and 2) (n = 4), looking away from the mobile for more than 2 consecutive min (n = 2), sickness ( n = 3), or experimenter error (n = 2).

Subjects were randomly assigned to one of 12 experimental groups (n = 6 each) that were differentiated in terms of the similarity between the training and test mobiles and bumpers (same, different) and the retention interval (1, 3, or 5 days). Thus, group lSmSb was tested with the same mobile and the same bumper after 1 day, group lSmDb was tested with the same mobile and a different bumper after 1 day, and so forth. Assignment of mobiles and bumpers during training and testing was counterbalanced within and across groups.


Appu ru f us During each session, the end and sides of the crib were lined with a brightly

colored cloth bumper to create a distinctive context. Two sets of bumpers that differed in both color and pattern were used. Each set consisted of two 122 cm x 144 cm side panels and a 66 cm X 122 cm end panel. One set was constructed of Kelly-green felt squares (5.08 cm2) separated by 5.08 cm in a grid pattern on bright yellow broadcloth [Figure l(a)]; the other was constructed of red broadcloth with perpendicular blue felt stripes, 2.54 cm wide, separated by 3.18 cm [Figure I(b)]. These patterns and color combinations were selected because they maximized the amount of edge and contrast and were not likely to be found in infants’ homes.

One of two mobiles, each composed of five painted wooden figures suspended on nylon string from an intersecting pair of rods, was used as the reinforcer. The mobile was hung from the tip of an L-shaped metal stand (BRS, S. Plainfield, NJ) that was clamped to the crib rail closest to the experimenter. A second stand was clamped directly opposite the first such that a second bar also projected over the center of the crib. One end of a soft white satin ribbon was looped around the infant’s ankle, and the other end was tied without slack to one of the two mobile stands. When the ribbon was connected to the stand from which the mobile was suspended [see Figures l(a) & l(b)], the mobile was activated in proportion to the rate and vigor of kicking (“conjugate reinforcement”). It has repeatedly been documented that the increase in response rate during a reinforcement period in this paradigm is not due to behavioral arousal but is under strict control of the instrumental contingency (Hill, Borovsky, & Rovee-Collier, 1988; Rovee & Rovee, 1969; Rovee-Collier, Morrongiello, Aron, & Kupersmidt, 1978).

Procedure Infants were tested in their home cribs at a time designated by their mothers

as an alert/play period. Although this time varied among infants, it was consistent over sessions for a particular infant. Each infant received two training sessions with a given mobile (the cue) and bumper (the context) on consecutive days (Sessions 1 and 2) and a test session (Session 3) either 1, 3, or 5 days later, depending upon group assignment. Training and test sessions were procedurally identical, differing only in the similarity of the mobile and bumper during training and testing. At one extreme, SmSb groups were tested with the same mobile and bumper that had been present during training; at the other, DmDb groups were tested with a mobile and bumper different from those during training. The remain- ing groups were tested with the same mobile and a different bumper (SmDb) or vice versa (DmSb).

All sessions lasted 15 min. Each session began with the serial introduction of the bumper, the nonmoving mobile, and the contingency, and concluded with their serial withdrawal in reverse order. At the outset of each session, the infant was placed supine in the crib by the mother and was allowed at least a I-min

Fig. 1. The experimental contexts in which training occurred: either (a) a yellow bumper with green squares or (b) a red bumper with blue stripes. Both 3-month-olds are shown during an acquisition phase (ribbon linking ankle to mobile suspension hook).


exposure to the bumper, which was already in place. Next, the mobile was hung from the stand to which the ankle ribbon was not attached for 3 min. During this initial nonreinforcement phase, the mobile was in view but could not be activated by kicks. Following this, the end of the ribbon was moved to the stand from which the mobile hung, and all kicks were conjugately reinforced for 9 min (acquisition). This was followed by a 3-min nonreinforcement period during which the ribbon was returned to its original position on the “empty” mobile stand while the mobile remained in place but stationary. Finally, the mobile was removed from the stand, and only the bumper was left in view. After 1 min, the mother removed her infant from the crib, and the session was over.

The mean number of kicksiminute during the 3-min nonreinforcement period at the outset of Session 1 (the baseline phase) defined the infant’s pretraining operant level. The mean number of kickdmin during the 3-min nonreinforcement period at the end of Session 2 (the immediate retention test phase) provided a measure of the infant’s retention after no delay. The mean number of kickshin during the 3-min nonreinforcement period at the outset of Session 3 (the long-term retention test phase) provided a measure of the infant’s responding after delays of 1, 3, or 5 days, prior to the reintroduction of the response-reinforcement contingency. A decrement in response rate from the immediate retention test to the long-term retention test could be due either to the retention interval per se or to changes in the cue, the context, or both at the time of the long-term test.

The experimenter stood out of direct view of the infant and recorded the number of kickshin. If the infant looked away or cried for more than 2 consecutive min, the session was stopped. A kick was defined as a complete horizontal or vertical excursion of the foot with the attached ribbon that at least partially re- traced its original path in a smooth, continuous motion (Rovee & Rovee, 1969). A second observer, naive with respect to the infant’s group assignment, indepen- dently recorded responses of eight different infants in 14 sessions. The Pearson product-moment correlation coefficient, computed over pairs of mutual observa- tions in corresponding min of each session, was 0.92.

Results Kicks/min were averaged across 3-min blocks for each infant, and separate

one-way analyses of variance were performed over the mean kick rates of the 12 independent test groups during the baseline phase (Block 1, Session 1) and the immediate retention test phase (Block 5 , Session 2). These analyses indicated that the groups did not differ either prior to or following the conclusion of training. Therefore, differences in performance during the long-term retention test did not arise prior to the introduction of the different experimental manipulations.

Performance during the long-term retention test in Session 3 was analyzed in terms of the two individual response measures, retention ratios and baseline ratios, that we have used in all previous studies of infant memory (for reviews, see Rovee-Collier & Fagen, 1981, and Rovee-Collier & Hayne, 1987). The baseline ratio (BIP) expresses the extent to which an infant’s response rate during the 3- min long-term retention test at the outset of Session 3 (B) exceeds that same infant’s unlearned response rate during the 3-min baseline phase at the outset of


Session 1 ( P ) . If a baseline ratio does not exceed 1.00, then the infant has responded at operant level during the test and has displayed no retention. A baseline ratio of 1.5 (equivalent to the learning criterion, i.e., responding at a rate 1.5 times operant level) is taken as evidence of retention by an individual infant.

The retention ratio (BIA) expresses the fraction of an infant’s mean response rate during the immediate retention test (A) that the same infant produces during the long-term retention test (B). A retention ratio of 1.00 or greater indicates that the infant’s response rate did not change from the immediate to the long-term retention test (i.e., perfect retention); lower retention ratios indicate greater pro- portional decrements in responding during the long-term test. This index permits determination of intermediate degrees of retention: Although a group may exhibit a significant retention deficit (i.e., their retention ratio is significantly less than a theoretical retention ratio of 1.00), their forgetting may not be complete (i.e., their baseline ratio is significantly above a theoretical baseline ratio of 1.00).

The means and standard errors of the baseline and retention ratios for each test group are presented in Table I . Mobile (2) X Bumper (2) x Retention Interval (3) analyses of variance over the mean baseline and retention ratios indicated that both ratios were higher when infants were tested with their training (“same”) mobile than with a different one [baseline ratio: F(1,60) = 15.88, p < .0002; retention ratio: F(1,60) = 9.20, p < .004]. In addition, baseline ratios were higher overall when infants were tested with the same bumper than with a different one [F(1,60) = 4.82, p < .03]. A significant Bumper x Retention Interval interaction in the retention ratio analysis [F(2,60) = 3.72, p < .03] reflected the fact that a different test bumper had no effect on retention ratios of groups tested after 1 day but reduced retention ratios after 5 days (Duncan’s multiple range test, p = .05).

Although analyses of variance reveal whether groups in the different test conditions differ, they do not provide a yesIno answer to the question of whether any given group exhibited retention during the long-term test. Groups may not have differed, for example, yet some or all may have remembered, or some or all may have forgotten. To answer this question, we used directional t-tests to com- pare each group’s mean baseline and retention ratio with its corresponding theoretical mean of 1.00 (no retention or perfect retention, respectively). Figure 2 summarizes the relation between the mobile (the cue) and the bumper (the context) over time.

Analyses of the mean baseline ratios indicated that groups tested with the same mobile and the same bumper exhibited significant retention after all intervals [Group 1SmSb: t ( 5 ) = 4.14, p < .007; Group 3SmSb: t(5) = 3.39, p < .005; Group SSmSb: t ( 5 ) = 4.84, p < .005], whereas groups tested with a different mobile and a different bumper performed at operant level after all delays. Except for Group lSmDb [ t ( 5 ) = 5.14, p < .05], groups whose test combination included either a different mobile or a different bumper performed at operant level after all delays.

Analyses of the mean retention ratios confirmed this result. All groups tested with the same mobile and same bumper except Group lSmSb had retention ratios not different from 1.00 after all delays. Although the retention ratio of Group lSmSb was high, as expected, and similar to ratios typically obtained 24 hr after training (Rovee-Collier & Fagen, 1981), it was significantly below 1.00 [ t (5) = 2.38, p < .04]. We attribute this to the fact that their standard error was unusually


1 1 0 -

1.00

0.90

0 I- ; 0.80

z

5 0.70 w I- w

0

IL: 0.60

0.50

TABLE I , Mean Baseline Ratios (BR) and Retention Ratios (RR) of Indepen- dent Groups of 3-Month-Olds Tested with One of Four CuelContext (Mobile1 Bumper) Combinations After Retention Intervals of 1 , 3, or 5 Days.

-

-

-

-

-

-

Retention Interval

1 Day 3 Days 5 Days Test Groups M (S.E.) M ( S . E . ) M ( S . E . )

SmSb BR RR

SmDb (Exp. 1A) BR RR

SmDb (Exp. 1B) BR RR

BR RR

BR RR

DmSb

DmDb

2.53* 0.81'

(0.37) (0.08)

2.74* 1.08

(0.52) (0.16)

1.70* 0.83

(0.14) (0.11)

2.09* 0.98

(0.24) (0.18)

1 .50 0.62+

(0.61) (0.16)

1.36 0.51'

(0.50) (0.11)

2.12* 1.14

(0.34) (0.17)

1.11 0.58+

(0.24) (0.13)

1.49 0.59+

(0.41) (0.07)

1.34 0.62+

(0.18) (0.24)

1.29 0.58'

(0.19) (0.11)

0.96 0.53+

(0.14) (0.08)

0.96 0.55+

(0.13) (0.03)

* BR significantly greater than 1 .OO (i.e., significant retention). - KR significantly less than 1.00 (i,e., significant retention deficit).

1 2 3 4 6

RETENTION INTERVALS (DAYS)

Fig. 2. Mean retention ratios of the 12 independent test groups in Experiment IA as a function of the retention interval. Infants were tested in the presence of the same mobile and the same bumper (SmShc solid c,ircles), the same mobile and a different bumper (SmDb: solid squares), a different mobile and the same bumper (DmSb: open circles), or a different mobile and a different bumper (DmDh: open squares). The retention ratios of groups with baseline ratios significantly greater than 1.00, indicative of retention, are starred.


small, being only half that of the other SmSb groups and also of group lSmDb, whose mean retention ratios were comparable but were not significantly less than 1.00 (see Table 1). Similarly, all groups tested with a different mobile and a different bumper had retention ratios significantly below 1 .OO after all delays [Group 1DmDb: t ( 5 ) = 3.93, p < .008; Group 3DmDb: t (5) = 5.66, p < .002; Group SDmDb: t ( 5 ) = 15.50, p < .0005].

The finding that infants tested with a different mobile and the same bumper performed at operant level after a l-day retention interval [lDmSb: t (5) = 3.17, p < .015] was predicted from previous work (Rovee-Collier & Sullivan, 1980), but the finding that infants did not generalize to a novel test mobile after retention intervals of 3 and 5 days [Group 3DmSb: t (5 ) = 5.76, p < .002; Group SDmSb; t ( 5 ) = 2.01, p < .04] was totally unexpected. Finally, the finding that infants who were tested with the original mobile in the presence of a different bumper exhibited no retention after delays of 3 or 5 days [Group 3SmDb: t ( 5 ) = 2.68, p < .035; Group 5SmDb: t ( 5 ) = 4.54, p < .004] was consistent with our earlier observation after 7 days (Rovee-Collier et al., 1985).

Figure 3 presents the mean kick rates during training (Sessions 1-2) and testing (Session 3). A Mobile (2) X Bumper (2) X Retention Interval (3) X Blocks (5 ) analysis of variance over kick rates during Session 3 yielded no main effects of any variable except Blocks. Responding increased over successive blocks [F(4,240) = 26.58, p < .0001], improving significantly in Block 2 when reinforcement was reintroduced (Duncan’s multiple range test, p = .05). Reacquisition was more rapid overall with the original training mobile than with a different one [F(4,240) = 3.10, p < .016]. Even after the sixth min of Session 3, infants were still responding significantly less to a different mobile than to the original training mobile. This difference disappeared during the final three blocks of Session 3 ; as a result, the main effect of Mobile only approached significance [F(1,60) = 3.89, p < .053]. The fact that response rates of all groups were high and equivalent by the end of Session 3 indicated that the low baseline and retention ratios of some groups during the long-term retention test were not due to poor motivation, illness, etc., on the test day.

Finally, we inquired whether any of the groups exhibited savings effects in Session 3 . Positive savings effects (better performance during reacquisition) are rarely obtained in studies with the mobile conjugate reinforcement paradigm because original learning is so rapid. Tests with novel mobiles, however, have occasionally resulted in poorer performance during reacquisition, or a “negative” savings effect (e.g., Rovee-Collier & Sullivan, 1980). To answer this question, a three-way analysis of variance was performed over the difference in responding during original acquisition in Session 1 and reacquisition during Session 3 (total kicks in Blocks 2-4 of Session 3 minus total kicks in Blocks 2-4 of Session 1) for factors of Mobile (2), Bumper (2), and Retention Interval ( 3 ) . This analysis yielded significant main effects of Bumper [F(1,60) = 5.37, p < .05] and Retention Inter- val [F(2,60) = 3.28, p < .05]. Duncan’s multiple range tests ( p = .05) revealed a significant negative savings effect for groups retrained with a different bumper and a significant positive savings effect for groups retrained with the same bumper. Similarly, a significant positive savings effect was observed after retention intervals of 1 and 5 days, but a negative savings effect was obtained after the 3-day

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retention interval. The main effect of Mobile was not significant, and there were no significant interactions.

Experiment 1B The finding that a contextual change did not impair retention 1 day after

training was surprising. This result was contrary to expectations and inconsistent with previous findings that the effect of a contextual change is greatest closest in time to training (Riccio et al., 1984). Before drawing conclusions regarding the temporal course of cue-context interactions, therefore, we thought it prudent to establish whether this result was replicable. To this end, the experimental conditions of Group lSmDb were repeated in Experiment 1B.

Method

Subjects and Procedure Six female infants (M = 87.7 days, SD = 5.7), recruited as before, were

trained and tested in a fashion identical to that of infants in Group 1SmL)b in Experiment 1A. Testing of one additionalinfant who cried for more than 2 consecutive min was discontinued. Data were collected by a trained experimenter who was unaware of the original study and blind to the basis for the present one.

Results Directional t-tests were performed between the mean baseline ratio and mean

retention ratio of replication Group 1 SmDb and their corresponding theoretical baseline and retention ratios of 1 .OO, respectively. As in Experiment lA, the mean baseline ratio was significantly above 1.00 [ t (5 ) = 3.29, p < .025], and the mean retention ratio was not significantly below 1.00 (see Table 1).

These data replicate the original result. Test performance after a 1-day retention interval was not impaired by a change in context. These data also confirm that 3-month-olds did not treat each different cue/context combination as a unique configuration but responded to the cue and the context as separable elements of a compound.

Discussion The findings of Experiment 1A are inconsistent with previous findings in two

respects. First, Rovee-Collier and Sullivan (1980) found that 3-month-olds progressively generalized to a novel test mobile as the retention interval increased from 1 to 5 days. Their conclusion that infants forgot the details of their training mobile more rapidly than its general features is in agreement with conclusions from studies of adult verbal learning and memory (Coll, 1985; Hasher & Griffin, 1978). In the present study, however, infants exhibited no responding to a novel test mobile after any of these same retention intervals. In the earlier study, infants had been trained and tested in the familiar context of their own cribs; in the


present study, they were trained and tested in a highly distinctive context. We conclude, therefore, that provision of a distinctive training context, unique to the training episode, was responsible for the differences in these results.

Second, the findings of Experiments 1A and 1B are inconsistent with previous reports that a contextual change impairs retention most strongly closest in time to training and that its debilitating effect progressively declines thereafter (for review, see Riccio et al., 1984). Although this description characterized the effect of a change in the visual characteristics of the mobile when 3-month-olds were trained in a setting in which a highly distinctive context was not explicitly provided (Rovee-Collier & Sullivan, 1980), it did not characterize the effect of a contextual change in the present study, when infants were trained in a highly distinctive setting that was encountered only during a training episode.

In both instances, the effect of training in a highly distinctive context was to buffer against generalized retrieval after longer delays (3 and 5 days), when responding was otherwise expected. We think that the present results reflect the documented role of the context as a memory prime (Rovee-Collier et al., 1985) and its effect on the memory contents at the time of the retention test (see also Gordon, 1981). Most authorities agree that when a subject attends to a stimulus or probe item (including, for humans with language, a question) at the time of testing, similar information that has previously been encoded is temporarily activated and compared with the contemporaneous physical stimulus, enabling a response to be given (Anderson & Bower, 1973; Lewis, 1979; Shiffrin & Schneider, 1977; Wagner, 1976, 1978). If the memory attributes that represent the specific details of the mobile are active, for example, then infants will respond only to the original mobile (or one almost identical to it); if only memory attributes representing general features of the mobile are active, however, then infants will respond to any mobile that shares these general features (Enright, 1981; Hayne, Rovee- Collier, & Perris, 1987; Rovee-Collier & Sullivan, 1980).

The discovery that generalization in Experiment 1A was forestalled after delays when it had previously been observed suggests that the distinctive context served to prime the otherwise inactive memory attributes representing the specific details of the mobile, returning them to an active state. Had the memory attributes representing the specific details of the mobile not been restored to an active state at the time of the 3- and 5-day retention tests, infants would have responded to the novel mobile after these delays; that is, memory retrieval would have proceeded on the basis of shared general features. Priming effects of pretest cues have been reported in previous studies of both human infants (Enright, Rovee-Collier, Fa- gen, & Caniglia, 1983; Fagen & Rovee-Collier, 1983) and animals (Gordon, 1981; Wagner, 1976; 1978).

We propose that the initial presentation of the context in the present study primed or activated the complete memory representation (including the details) of the succeeding cue which, one accessed, activated the memory of the response- reinforcement contingency (or of the response requirement? see Gordon & Spear, 1973), enabling the infants to respond appropriately. After a delay of only 1 day, the initial priming effect of the context could not be distinguished from the retrieval function of the cue because presentation of the cue alone was still capable of accessing the complete memory representation after that delay. For the same


reason, a contextual change did not disrupt retention after a I-day delay as long as the original cue was present. After delays of 3 days and longer, however, when the cue could access memory attributes representing only its general features, the priming function of the context was revealed: If the original context was present during testing, infants responded to the original mobile and to no other; if the test context was different, infants appeared not to recognize the original mobile but stared at it “blankly” without responding.

These findings suggest that the context functions as an initial attention gate for the retrieval of the memory representation of the cue after longer delays. “Gat- ing” refers to the notion that attention to potential retrieval cues must be filtered or screened at one level before it can be channeled to potential retrieval cues for filtering or screening at the next level. The general model of attention gating was first introduced by Reeves and Sperling (1986). They assumed that detection of the visual target in an initially encountered set of information triggered the opening of an attention gate that let subsequently attended visual information enter a short- term memory store. Information persisted in the short-term visual store without forgetting until a response based on that information was made. When serially presented stimuli required attentional shifts between different spatial locations in the visual field, a series of attention gates were assumed to open and close, first at one location (the expected location of the initial target) and then at another (the expected location of the next set of cues). The first gate had to close before the second gate opened. This gating function shares many similarities with an occasion-setting function of the context (Holland, 1985).

Although the present experiments are vastly different from those on which the original model was based, the concept of attention gating is consistent with the conclusion that what the subject notices in the test situation determines what previously encoded information is retrieved or activated (Lewis, 1979; Spear, 1973). According to this account, detection of appropriate retrieval cues in the context opens the first retrieval gate, allowing its memory representation to enter a short-term or active memory store, and the gate then closes. This permits attention to flow to the focal cue. Detection of effective retrieval cues in the focal cue opens the second retrieval gate, allowing its (complete) memory representation to enter the short-term or active store, and the gate then closes. Activation of the memory representation of the cue is prerequisite for accessing the subject’s memory of the contingency (or response requirement) and enabling the response to be made. If the context is novel and the first gate does not open, the retrieval process is aborted at that point. Even if the context is the same and the first gate opens and closes, if the subsequently attended cue is novel, then the second gate cannot open, and the retrieval process will be aborted at that point. The resulting retrieval failure will be seen as poor retention test performance.

This analysis accounts for the failure of infants to generalize to a novel mobile in the distinctive original context after longer delays in Experiment 1A as they had done in the Rovee-Collier and Sullivan (1980) study when a distinctive context was not provided. Only if the memory attributes representing the specific details of the cue were activated, presumably by the context, could infants exhibit discrimination of the novel test mobile after delays of 3 days and longer. Conversely, the finding that infants were unaffected by a contextual change after 1 day if the


original cue was present during testing suggests that as long as the specific details of the mobile are highly accessible, attention to those details assumes precedence over attention to more peripheral contextual information. As a result, the initial attention gate can be bypassed. Whether such attentional precedence is unique to very young infants or characterizes attention across the infancy period is a problem for future research.

Experiment 2

The second experiment was designed to determine whether the gating function attributed to the context and cue would predict the efficacy of cue/context combinations as reminders in a reactivation paradigm. It has been well-documented for both animal infants (Campbell & Jaynes, 1966; Richardson, Riccio, & Axiotis, 1986; Richardson et al., 1988; Spear & Parsons, 1976) and human infants (for review, see Rovee-Collier & Hayne, 1987) that a brief exposure to a retrieval cue (some aspect of the original training episode) prior to a long-term retention test can restore subsequent test performance to the level previously observed immediately after training. The reminder presumably primes or reactivates the dormant or inaccessible memory of training (Spear, 1973; 1978).

The test stimuli in a reactivation paradigm differ from those in the simple forgetting paradigm of Experiment 1 A, when different groups were tested with either the same cue/context combination or one of its variants 24 hr after training. In the reactivation paradigm, all groups are tested with the original cue/context combination 24 hr after the reminder; here, the reminder is either the original cue/ context combination or one of its variants. In the past, we have found that stimuli that do not cue retrieval 24 hr after training are also ineffective reminders (e.g., Hayne et al., 1987). However, not all stimuli that are effective retrieval cues 24 hr after training, when the memory is still highly accessible, are able to reactivate a memory that has become inaccessible (Rovee-Collier & Hayne, 1987).

Method

Subjects and Apparatus

Subjects were 18 infants (9 males, 9 females) with a mean age of 86.0 days (SD = 4.2). Infants were recruited as before and assigned to one of three reactivation conditions (n = 6 each) as they became available for testing. Additional infants were excluded as a result of crying continuously for 2 min during any session (n = 9), failure to meet the learning criterion (n = l), experimenter error (n = l ) , or scheduling problems (n = 1).

The three groups (React SmSb, React SmDb, React DmSb) differed only in the mobile/bumper combination presented as a reminder during the reactivation treatment. These were the same combinations used during the l-day retention test in Experimenter 1A except that the differentidifferent combination was omitted. For all three groups, the original mobile and original bumper were present during the long-term retention test. The mobiles and bumpers were counterbalanced within and across groups as nearly as possible.


Procedure All infants were trained and tested in a fashion identical to that of the SmSb

group in Experiment 1A with the sole exception that Session 3 occurred after a retention interval of 2 weeks. This retention interval was selected because 3- month-olds trained in an identical procedure either with (Hayne, 1988; Rovee- Collier et al., 1985) or without (Fagen & Rovee-Collier, 1983; Sullivan, Rovee- Collier, & Tynes, 1979) a distinctive context exhibit forgetting 6-8 days after training.

One day prior to the long-term retention test (13 days following Session 2), infants in all reminder groups were placed in a sling seat inside their cribs for a 3- min reactivation treatment. The sling seat minimizes unlearned activity during the presentation of the reminder (Sullivan, 1982) and does not affect subsequent retention (Fagen & Rovee-Collier, 1983). One end of the ribbon was tied to the stand from which the mobile hung, and the other was held by an experimenter, con- cealed from the infant’s view, who moved the mobile in each of the 3 min the same number of times that a given infant had kicked during each of hidher last 3 min of acquisition in Session 2.

We emphasize that the 3-min reactivation treatment was the only point in the procedure at which the three groups were treated differently; in Session 3, all groups were tested with the same mobile/bumper combination that had been present during training.

Results and Discussion The mean response rates of the three groups during training (Sessions 1 and 2)

and testing (Session 3) are presented in Figure 4. A one-way analysis of variance indicated that the groups initially differed in

operant level [F(2,15) = 4.46, p < .03]. A Duncan’s multiple range test (p = .05) indicated that the operant level of Group React SmSb ( M = 14) was significantly higher than that of Group React SmDb ( M = 6); the operant level of Group React DmSb ( M = 8), however, was not different from that of the other groups. As in Experiment lA, however, the groups did not differ during either training or the immediate retention test at the conclusion of training, and all met the learning criterion in Block 2 of Session 1.

A Groups (3) x Blocks (5 ) analysis of variance with repeated measures over Blocks was performed over the absolute kick rates of Session 3 (Figure 4, right panel). Only the main effect of Blocks was significant, [F(4,60) = 27.97, p < .0001], indicating that infants were responsive to the reintroduction of the response-reinforcement contingency. As before, then, poor performance on the part of some groups during the first 3 min of Session 3 were not attributable to poor motivation, illness, etc., during the 2-week test.

Mean baseline and retention ratios are presented in Table 2. As can be seen, the effectiveness of the different cue/context combinations as reminders was predicted by their effectiveness as retrieval cues in Experiment 1A.

Directional t-tests indicated that only Group React SmSb exhibited no forgetting during the 3-min long-term retention test. Their mean baseline ratio was significantly greater than 1.00 [ t (5) = 2.12, p < .05], and their mean retention ratio


uo

T MOBILE BUMPER

REACT

" , : , " , E z U M P E R

REACT DIFFERENT MOBILE SAME BUMPER

1 2 3 4 5 1 2 3 4 5

3-MIN BLOCKS

1 2 3 4 5

Fig. 4. Combined learning curves of 18 infants in three reactivation groups during two training sessions (left panels) and of each reactivation group ( n = 6) in Session 3 (right panels), 24 hr following a reactivation treatment with one of three cue/context (mobileibumper) combinations: SmSb (dotted line), SmDb (solid line), or DmSb (slashed line). Session 3 occurred 2 weeks following the conclusion of Session 2. In Session 3, all infants were tested with their original mobile and bumper. In all sessions, reinforcement was available only in Blocks 2-4. Retention was measured in Block I of Session 3 (the long-term retention test phase), prior to the reintroduction of reinforcement.

was not significantly less than 1.00. In contrast, infants whose reminder contained a different cue (React DmSb) exhibited no retention at all. Their mean baseline ratio was not significantly above 1.00, and their mean retention ratio was significantly less than 1.00 [t(5) = 3.92, p < .008]. Their test performance was not different from that of identically trained infants receiving no reminder at all (Hayne, 1988; Rovee-Collier et al., 1985). Infants reminded with the original cue in a different context (React SmDb) had a low retention ratio that was significantly less than 1.00 [ t (5 ) = 3.94, p < .008]. Their mean baseline ratio, however, was significantly above 1.00 [ t (5 ) = 2.58, p < .03], indicating that they did exhibit some retention. This result suggests that a different context only modulates the effectiveness of the original cue as a reminder. This conclusion, however, must be viewed with caution because the low operant level of Group React SmDb could have contributed to this result. In fact, the response rate of this group during the long-term test (Block 1, Session 3) did not differ from that of Group React DmDb (see Figure 4). In a recently concluded extension of this work, we have found that


TABLE 2. Mean Baseline Ratios (BR) and Retention Ratios (RR) of Three Cue1 Context (MobilelBumper) Reactivation Groups.

~ ~ ~~ ~~ ~

Test Groups M ( S . E . )

SmSb BR 1.35* (0.16) RR 0.94 (0.25)

BR 2.36* (0.50) RR 0.72+ (0.07)

BR 1.06 (0.12) RR 0.53' (0.12)

SmDb

DmSb

~~~~ ~ ~

* BR significantly greater than 1.00 (i.e., sig-

+ RR significantly less than 1.00 (i.e., signifi- nificant retention).

cant retention deficit).

3-month-olds who are trained and tested in their own crib exhibit no retention during the long-term test if reminded with their original mobile in locations other than where they were trained. Whether the effect of altering the reminder context was partial or complete, however, it significantly impaired retention.

The results of Experiment 2 confirmed our prediction that stimuli that are effective retrieval cues 24 hr after training are usually effective reminders after longer delays, but stimuli that are ineffective in cueing retrieval after a 24-hr delay are not (Hayne et al., 1987; Rovee-Collier & Hayne, 1987). In addition, the results are consistent with the hypothesis that attention to effective retrieval cues is sequentially screened or gated, first at the level of the context and then at the level of the cue. At each level, the process leading to the ultimate retrieval of the response-reinforcement contingency (or the response requirement) can be aborted. In the Reeves and Sperling (1986) attention-gating model, although detection of the initial target on each trial triggered the opening of an attention gate that let subsequently attended visual information enter a short-term memory store, this process was not all-or-none. Rather, the amount of information that entered the active store was thought to depend on how wide the gate was opened. In the present study, the SmDb cue/context combination could have produced an analo- gous effect, only partially opening the first attention gate and therefore providing a weak reminder that only partially alleviated forgetting.

In addition, the findings of both experiments provide convergent evidence for the conclusion of Richardson et al. (1988) that memories of very young organisms include information about the context in which an event occurs and, more impor- tant, that the retrieval of both recently acquired and forgotten memories is highly specific to the similarity between the contextual cues that were originally encoded and those active at the time of retrieval. This evidence suggests that the prevailing view that immature animals and human infants are incapable of processing con-


textual information (Nadel et al., 1985; Nadel & Zola-Morgan, 1984; Schacter & Moscovitch, 1984) must be reassessed.

Notes This research was based on a master’s thesis completed by the first author under the direction of

the second. Portions of the data were presented at the meeting of the Eastern Psychological Associa- tion, New York City, April 1986. The research was supported by Grant MH32307 awarded to the second author from the National Institute of Mental Health. We thank Mark Bouton, Michael D’ Amato, Charles Flaherty, Arthur Tomie, and Arlene Walker-Andrews for suggestions and criticisms of an earlier draft of the manuscript, Harlene Hayne for assistance with the data analysis, and Linda Earley for collecting the data for Experiment 1B.

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