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Short-term visual recognition and temporal order memory are both well-preserved in aging Volen National Center for Complex Systems, Brandeis University ‡Department of Psychology, University of Pennsylvania Volen National Center for Complex Systems, Brandeis University For correspondence, e-mail: sekuler/at/brandeis.edu The publisher's final edited version of this article is available at Psychol Aging. See other articles in PMC that cite the published article.Abstract Increased difficulty with memory for recent events is a well-documented consequence of normal aging, but not all aspects of memory may be equally affected. To compare aging's relative impacts on short-term recognition and temporal order memory, young and older adults were asked to identify the serial position that a probe item had occupied in a study set, or to judge that the probe was novel (had not been in the study set). Stimuli were compound sinusoidal gratings, which resist verbal description and rehearsal. With retention intervals of 1 or 4 seconds, young and older adults produced highly similar results, including overall performance levels, serial position curves, and the proportion of trials on which a correct recognition response was accompanied by an incorrect temporal order judgment. Temporal order errors, which occurred on about one quarter of trials, were traced to two factors: perceptual similarity between the wrongly identified study item and the correct study item, and temporal similarity between the wrongly identified item and the correct one. Our results show that short-term visual temporal order memory is well-preserved in normal aging, and when temporal order errors do occur, they arise from similar causes for both young and older people. Keywords: Aging, short-term visual memory, temporal order memory, recognition, identification Increased difficulty with memory for recent events is among normal aging's best known and most harmful consequences (Kausler, 1994; Wingfield & Kahana, 2002). However, it is clear that not all dimensions of short-term memory are equally vulnerable to age-related changes (for example, McIntosh et al., 1999; Olson et al., 2004). Source memory (Johnson, Hashtroudi, & Lindsay, 1993), which includes information about the temporal order in which items were recently encountered, seems to be particularly vulnerable to the effects of aging (Newman, Allen, & Kaszniak, 2001; Fabiani & Friedman, 1997; Kahana, Howard, Zaromb, & Wingfield, 2002), (but see, Siedlecki, Salthouse, & Berish, 2005). To explore this question further, we examined both visual short-term recognition memory and visual short-term temporal order memory, using rehearsal-resistant (Hwang et al., 2005) sinusoidal gratings as study and test items, and taking care to equate each participant's stimuli on the basis of visual discriminability. Recent studies with such stimuli, revealed a striking preservation of short-term, item recognition memory with aging (Della-Maggiore et al., 2000; Bennett, Sekuler, McIntosh, & Della-Maggiore, 2001; McIntosh et al., 1999). For example, Sekuler, Kahana, McLaughlin, Golomb, and Wingfield (2005) showed that young and older participants demonstrated equivalent short-term visual recognition memory, achieving equivalent proportions of correct “old”-“new” judgments, at each of three different, brief test delays. The present study adapted these basic methods to examine short-term temporal order memory with a new sample of participants. In addition, we exploited the metric properties of the grating stimuli in order to identify deterministic causes of observed errors in short-term temporal order memory. On each trial in our study, participants saw a series of three compound gratings followed by a probe (test) grating. These stimuli were used, in part, because of their resistance to consistent verbal labeling and rehearsal (Della-Maggiore et al., 2000; Hwang et al., 2005). This attribute made it possible to examine short-term visual memory with minimal contamination from verbal mediation. At the end of each trial, participants judged whether a probe item had been in the study series, and, if so, which study item it had been, first, second or third. Because judgments of item familiarity (“old”/“new”) and judgments related to temporal order can be differentially affected by even short delays in testing (Yonelinas & Levy, 2002) we made measurements with two different retention intervals. Our questions were first, whether short-term visual memory for item familiarity was better than short-term visual memory for temporal order information, and second, whether these aspects of visual short-term memory might be preserved in aging, in contrast to other aspects of memory, including verbal memory (for example, Kahana et al., 2002). Methods Procedure On each trial, a study series comprising three compound sinusoidal gratings was followed by a probe stimulus (p). Each of the three study stimuli (s1, s2, and s3) was presented for 750 ms, separated by inter-stimulus intervals of 400 ms each. Then, after a delay of either 1000 or 4000 ms, a warning tone sounded, and p was presented for 750 ms. Participants then used a response selection display to indicate whether p had been in the study set, and, if it had been in the set, which of the three study items it matched. We refer to a p that matched one of the study items as a target, and a trial on which p matched a study item as a target trial. We designate a non-matching p as a lure, and we designate trials on which p matched none of the study items, a lure trial. Target and lure trials occurred in random order, in a ratio of 3:1. For lure trials, stimuli were selected by randomly sampling four items (three study and a p) without replacement from the entire pool of 25 stimuli. For target trials, the three study items were randomly selected from the pool of 25 stimuli, but the choice of p was constrained so that it matched one of the three study items in the study series, and did so equally often for items in the first, second or third serial positions. On each trial, after p disappeared, a response selection screen was presented on the computer display, and remained visible until the participant made a response. The selection screen displayed four alternatives, labeled “None,” “First,” “Second,” or “Third.” Participants used the computer mouse to select the alternative that corresponded to the serial position (first, second, or third) of the study stimulus, s1, s2, or s3, which matched p. If p seemed to have matched none of the study items, the participant clicked on the alternative labelled ”None.” No instructions were given about response speed. Distinctive tones provided feedback after each response. On target trials, feedback was contingent upon the response's identification component: feedback signalled whether the participant's response correctly identified which study item, s1, s2, or s3, matched p; like incorrect identification responses, a ”none” response on a target trial brought feedback that the response was wrong. On lure trials, feedback was contingent on whether the response correctly signified that none of the study items matched p; all other resonses, ”First,” ”Second,” or ”Third,” was followed by feedback that the response had been wrong. Prior to the experiment, participants were told the proportions of target and lure trials. Each participant was tested on 288 trials distributed across two one-hour sessions. In each session, participants completed a block of 72 trials with a pre-probe delay of 1 sec, and another block of 72 trials with a pre-probe delay of 4 sec. Designating these two conditions A and B, half the participants completed four blocks of experimental trials in an ABBA order, half in a BAAB order. Participants Ten young adults (19 - 25 years of age, M = 21.8, SD = 2.1) and ten older adults (65 - 80 years of age, M = 71.4, SD = 6.0) participated in this study for monetary compensation. Five of the young adults were male, five female; three of the older adults were male, seven female. Each participant's visual acuity was measured using Landolt C targets. Young participants' acuity ranged from 20/13 - 20/25 (M = 20/18.1, SD = 3.2) and older participants' acuity ranged from 20/22 20/40 (M = 20/31.7, SD = 7.2). Contrast sensitivity was measured with a Lighthouse Letter Contrast Sensitivity Test. Young participants' sensitivity ranged from 1.64 1.80 (M = 1.71, SD = 0.07) and older participants' sensitivity ranged from 1.28 - 1.68 (M = 1.56, SD = 0.12). To control effects of individual or age-related differences in vision, a participant's stimuli were scaled according to that participant's discrimination threshold for spatial frequency (Zhou, Kahana, & Sekuler, 2004). So before our memory experiment, a staircase procedure measured each participant's spatial frequency discrimination threshold for sinusoidal gratings. Threshold was defined as P=0.794 on the psychometric function. The timing of the stimuli corresponded to the timing that would be used in the memory experiment itself. The resulting Weber fractions ranged from 6.5 13.2% for young participants (M = 9.7, SD = 3.5), and from 8.2 - 26.0% for older participants (M = 16.7, SD = 6.6). The difference between group means was significant, (t(18)=-2.98, p <0.01). By self-report, all older participants were in good health, had good cognitive function, and had at least some college education. Older participants' score on the Mini-Mental State Examination ranged from 28 30, with a mean = 29.4, SD = .07, which exceeds the population-based norm of 28 for 65 - 79 year olds with college experience or an advanced degree (Crum, Anthony, Bassett, & Folstein, 1993). Stimuli Stimuli for each trial were drawn from a pool of compound sinusoidal gratings, each comprising superimposed vertical and horizontal sinusoidal luminance gratings. Details are given in Sekuler et al. (2005). The pool of stimuli for each participant was generated by crossing five vertical spatial frequencies with five horizontal spatial frequencies. Vertical as well as horizontal spatial frequencies were 2 cycles/degree ± 3× or 6× a participant's Weber fraction for spatial frequency. The gratings sinusoidal components had a Michelson contrast of 0.2, a value well above the threshold for detection. To minimize edges, stimuli were windowed by a circular 2-D Gaussian with space constant of 1 degree visual angle. The display's mean luminance was fixed at 17.8 cd/m2. Each participant viewed the stimulus from a distance of 114 cm, head supported and steadied by a head rest and chin cup. Trials were self-paced. By enforcing a minimum between-stimulus difference of 3× a participant's discrimination threshold, we reduced the likelihood that perceptual confusions between pairs of stimuli, with minimal memory load, could by themselves lead to misidentifications. With threshold defined by the P=0.794 point on the psycho-metric function, stimuli that differed by one threshold unit would be mistaken for one another with P= 1−0.794, or 0.206. By extrapolation, stimuli that differed by 3× threshold would be mistaken for one another 0.2063, or slightly less than 1% of trials. To check this simple prediction, a supplementary experiment tested five new participants, ages 18-27. With pairs of gratings whose spatial frequencies differed by 3× a participant's discrimination threshold, perceptual confusions did indeed occur on fewer than 1% of trials. Results Table 1 summarizes the principal measures used to characterize participants' mnemonic processes. The table's first line shows the proportion of correct identifications of serial position; that is, the proportion of trials on which the stimulus was st, where st {1, 2, 3}, and participants responded rt, where rt {1, 2, 3}. Table 1's second line gives the proportion of correct recognitions calculated without regard to identification of serial position. This is the proportion of trials on which participants responded either r1, r2, or r3 given st, aggregating cases in which the response was rt and cases in which it was not. The third row in the table gives a conditional value, rt | st, the proportion of trials on which both the recognition judgment (“yes”) and the identification of p serial position were correct. If every correct recognition had been accompanied by a correct identification, cells in row three would show P(Identification Recognition)=1. Target trials on which recognition was correct, but identification wrong constitute misidentifications, that is, errors in serial position judgment. The proportion of such trials can be obtained from the quantity 1–P(Identification|Recognition). The last line in Table 1 gives the proportion of all trials, right or wrong, on which participants judged that p had been in the study series. The difference between groups on this measure was not significantly different. For comparison, the actual proportion of target trials was 0.75.
The upper panels in Figure 1
Confirming what may be evident in the first and second lines of Table 1, Figure 1 Although recognition responses showed no statistically significant serial position effect, such an effect was manifest with identification responses, that is, when participants' serial position judgments were taken into account. This serial position effect was considerably diminished at the longer of our two retention intervals (F(2,36)=6.22, p <0.01). Errors in visual temporal order judgments can be exploited to identify the information that participants use to make successful judgments. This is especially true when, as is the case here, the metric properties of stimuli makes it possible to relate misidentifications to stimulus characteristics. For young participants, on 21% of trials when recognition was correct, the target was attributed to an incorrect serial position; for older participants, the corresponding value was 17%. The difference between the two age groups was not statistically significant (p>.40). Basically, misidentifications could have arisen from either of two quite distinct sources. Some or all of the misidentifications could have been entirely stochastic, reflecting random guesses made when participants had no actual useable memory of what had been seen. Alternatively, misidentifications could have come from some deterministic process, for example, systematic errors associated with partial loss of serial position information. We set out to evaluate these alternative accounts of misidentifications. To compare competing stochastic and deterministic accounts of misidentifications, each participant's misidentifications were sorted into the cells of a notional 2×2 table. In this sorting, we considered only trials on which p actually matched s1 or s3. The table's rows corresponded to two levels of a variable we call spatial similarity; the table's columns correspond to two levels of a variable we call temporal similarity. To generate the value of spatial similarity, we calculated the Euclidean distance in spatial frequency between (a) p and the misidentified study item, and (b) p and the remaining study item that did not match p. If the first of these two distances were the smaller, we categorized spatial similarity between p and misidentified item as “high”; otherwise, we categorized spatial similarity as “low.” For temporal similarity, we categorized misidentifications according to whether the error in identification represented a shift of one (high similarity) or two (low similarity) serial positions. For example, if s2 were misidentified as matching p, when the actual matching study item was s3, this error of one serial position was categorized as high temporal similarity; if s1 were misidentified as matching p, when the actual matching study item was s3, the error of two serial positions was categorized as low temporal similarity. A factorial cross of spatial and temporal variables produced four combinations of spatiotemporal differences between p and the misidentified study item. The proportions of all serial position errors that fell into each of the four categories are shown in Figure 1C The results shown in Figure 1C The distribution of misidentifications across the four categories in the notional 2×2 table suggests that both temporal and physical similarity induced temporal order errors, with physical similarity exerting a larger effect than temporal similarity (compare the pair of bars at the left side of Figure 1C Finally, we must comment on one deterministic process that had the potential to promote errors in short-term temporal order memory, but most likely did not: purely perceptual confusions among stimuli. Stimulus series were constructed so that any two study stimuli differed in spatial frequency by at least 3× a participant's difference threshold. As noted earlier, when visual stimuli differ by that much, perceptual confusion alone, with minimal contribution from errors in short-tem memory, would have caused the stimuli to be mistaken for one another less than 1% of the time. So perception-based mistaken identity alone cannot explain the much higher proportion of misidentifications, that is, the obtained values of 1–P(Identification—Recognition). Instead, for an explanation of misidentifications we must look elsewhere. Discussion Sensory researchers have long understood that perceptual errors, including illusions, can be a valuable source of insight into perception's normal operation (Eagleman, 2001). In the same way, from the very beginning of systematic research on memory, errors and failures have been useful in illuminating memory's normal operation (Schacter & Dodson, 2001). As Figure 1 To understand how spatial similarity might lead to errors in temporal order, we will use the basic structure of summed-similarity (or global-matching) memory models (Nosofsky, 1986; Clark & Gronlund, 1996; Kahana & Sekuler, 2002). We will work within this framework, because NEMo, one member of this class of models, has already accounted successfully for short-term memory with stimuli like those used here (Kahana & Sekuler, 2002). A summed similarity model assumes that the study items, s1 … s3, are stored in memory as corresponding noisy exemplars, m1 … m3, where the exemplars' subscripts signify the order in which the visual stimuli had been presented. When the probe, p, is presented, η1 …η3, the set of similarities between p and each of the noisy exemplars is computed. Again, subscripts signify the order in which study stimuli were presented. NEMo describes each similarity value as an exponentially decreasing function of the spatial difference between p and the corresponding values, m1 … m3. From the resulting similarity values, a summed similarity, Ση, is computed. Some criterion value of Ση > k is taken as evidence that at least one of the study items matched p, which makes p seem familiar. Over trials, the probability of a recognition response (that is, a “yes” response) corresponds to the proportion of trials on which Ση > k. The central role that noise can play in summed similarity models brings to mind the role it occupies in some theories of cognitive aging. For example, Welford (1984) offered the influential proposal that various age-related changes in performance reflected older adults' relatively higher levels of internal neural noise (random variability). Researchers have developed and deployed powerful computational methods for testing detailed descriptions of noise's role in short-term memory, distinguishing between different sources of noise, such as internal vs. external noise, and different forms of noise, such as multiplicative vs. additive noise (Gold, Murray, Sekuler, Bennett, & Sekuler, 2005), but such analyses have as yet not been applied to results from older adults. Because we intentionally tailored stimuli to individual participants' visual discrimination, it is impossible to tell from our data whether age-related differences in internal noise accompany visual encoding. But we can exploit the summed similarity framework to generate useful propositions about age-related noise in the context of short-term recognition and temporal order memory. First, consider how a summed similarity model could be extended to account for temporal order judgments. Such an extension requires that the model perform one additional operation on the set of similarities associated with a trial's study stimuli and p. In this additional operation, the similarities are processed with a max operator, which returns two values, the largest item {η1 …η3}, and the index (serial position) of that largest item. Hereafter, we refer to these returned quantities as value and index, respectively. The identification of the matching serial position is determined by the index, 1 … 3, returned by the max operator. Because of visual noise associated with each exemplar, there will be trials on which the index returned by max would not represent the serial position whose study item physically matched p, but would represent instead the serial position of another study item. On such trials, the model generates a temporal order error, in which the serial position of the matching item is misidentified. The probability of such errors will be some monotonically decreasing function of each study item's spatial frequency similarity to p. In other words, study items that did not match p but were spatially similar to it would be more likely misidentified as a match than would study items that were less spatially similar to p. Of course, this is the pattern of spatial similarity effects shown in Figure 1CSecond, consider how a different mechanism is required to motivate temporal similarity's influence on misidentifications of serial position. Drawing upon accounts of temporal effects in free recall (Howard & Kahana, 1999, 2002), we assume that the representation of each noisy exemplar is tagged in memory with a temporal code, and that each item's temporal tag could be misassigned at encoding, or degraded in memory by passage of time and/or interference. If this degradation were partial rather than complete (Dodson, Holland, & Shimamura, 1998), serially adjacent positions in a sequence would more likely be confused with one another than would be positions more widely separated in a sequence. In the case at hand, with partial loss of serial position information, s1 is more likely misremembered as s2 than as s3, and s3 is more likely misremembered as s2 than as s1. Again, this is the pattern of results seen in Figure 1C With the rapid presentations and relatively short retention intervals used in this experiment, it is not likely that by itself the passage of time was primarily responsible for degrading serial position information (e.g., Sekuler et al., 2005). Instead, interference in memory, generated by presentation of successive study items was more likely at fault. Whatever the details of such interference prove to be, the present results demonstrate a striking age invariance in both item and order short-term memory for visual gratings, which resist verbal labeling and rehearsal. This invariance stands in contrast to age-related differences in order memory with verbal material (Kahana et al., 2002). This divergence leads us to hypothesize that our results depend crucially upon test materials whose discriminability is equated between participants (Zhou et al., 2004) , and whose characteristics minimize participants' reliance on verbal labeling and rehearsal. Further speculation about our results' boundary conditions must await future research, however, it does seem that in spite of well-documented, age-related declines in other cognitive domains, the neural substrates underlying short-term visual memory remain robust, perhaps supported by compensatory reorganization of task-related cortical networks (McIntosh et al., 1999; Della-Maggiore et al., 2000). Acknowledgments Supported by NIH grants MH068404, MH55687 and AG15852, and by the W. M. Keck Foundation. We thank Feng Zhou for running the supplementary experiment on visual confusions between stimuli. References
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