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. 2012 Jul 24;109(30):12237-41.
doi: 10.1073/pnas.1209685109. Epub 2012 Jul 9.

Monkeys have a limited form of short-term memory in audition

Brian H Scott  1 , Mortimer Mishkin, Pingbo Yin
Affiliations

Monkeys have a limited form of short-term memory in audition

Brian H Scott et al. Proc Natl Acad Sci U S A. .

Abstract

A stimulus trace may be temporarily retained either actively [i.e., in working memory (WM)] or by the weaker mnemonic process we will call passive short-term memory, in which a given stimulus trace is highly susceptible to "overwriting" by a subsequent stimulus. It has been suggested that WM is the more robust process because it exploits long-term memory (i.e., a current stimulus activates a stored representation of that stimulus, which can then be actively maintained). Recent studies have suggested that monkeys may be unable to store acoustic signals in long-term memory, raising the possibility that they may therefore also lack auditory WM. To explore this possibility, we tested rhesus monkeys on a serial delayed match-to-sample (DMS) task using a small set of sounds presented with ~1-s interstimulus delays. Performance was accurate whenever a match or a nonmatch stimulus followed the sample directly, but it fell precipitously if a single nonmatch stimulus intervened between sample and match. The steep drop in accuracy was found to be due not to passive decay of the sample's trace, but to retroactive interference from the intervening nonmatch stimulus. This "overwriting" effect was far greater than that observed previously in serial DMS with visual stimuli. The results, which accord with the notion that WM relies on long-term memory, indicate that monkeys perform serial DMS in audition remarkably poorly and that whatever success they had on this task depended largely, if not entirely, on the retention of stimulus traces in the passive form of short-term memory.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Schematic diagram of the timing of a DMS trial. The animal initiated a trial by holding a contact bar for 300 ms. A sample stimulus (∼300 ms in duration) was presented, followed by one to three test sounds with a varied ISI of 800–1200 ms. When the test sound was the same as the sample (a match), the animal was required to release the bar within a 1,200-ms response window beginning 100 ms after match onset. A correct response (a “hit”) earned a liquid reward 300 ms after bar release. A response within the first 100 ms following match onset was considered an early release error. Failure to release by the end of the response window was counted as a “miss” error. If the stimulus following the sample was a nonmatch, the animal was required to hold the bar (a “correct rejection”) until the match stimulus was presented. Release to the nonmatch was counted as a FA error. Any type of error aborted the trial and was penalized by a 3-s time out in addition to the standard 3-s intertrial interval, to discourage animals from aborting trials with multiple nonmatches. Each trial ended after release of the bar, but if the bar was released during stimulus presentation, the full stimulus played out before the trial was reset. Trials with zero, one, or two nonmatch sounds were randomly generated with equal probability. In an attempt to aid the animal’s performance, the task was designed such that the nonmatch stimuli, which were selected pseudorandomly on each trial, did not belong to the same stimulus category as the sample. Trials were organized in blocks such that each stimulus in the set served as the sample in a pseudorandom order before the same stimulus was used again.
Fig. 2.
Fig. 2.
(A) Overall performance (mean +SD) as measured by proportion of correct trials (Left) and DI (Right) for all standard testing sessions (black bars, monkey F, n = 360 sessions, >250,000 trials; gray bars, monkey S, n = 116 sessions, >82,000 trials). (B) Hit rate, FA rate, and DIs computed separately at each position within the trial sequence for monkey F (black) and monkey S (gray). FA rate and DI are not computed for the fourth stimulus, because it is always a match, and so no FA can occur (details in SI Methods, Analysis of Behavioral Performance and Fig. S3). (C) Control task 1 with variable ISIs between sample offset and match onset. Performance is plotted as a function of the total sample-match interval (e.g., a one-nonmatch trial at an ISI of 0.5 s would include two 0.5-s delay intervals plus the 0.3-s duration of the intervening nonmatch stimulus, for a total of 1.3 s) and is shown separately for trials with (i) no nonmatch stimulus (upper curves) and (ii) one intervening nonmatch stimulus (lower curves). In the absence of a nonmatch stimulus, DMS performance in both animals is stable up to 3 s. With a single intervening nonmatch stimulus, scores at 1- and 2-s intervals are significantly below those without an intervening nonmatch, and there is a strong effect of delays ≥4 s. Asterisks mark scores that are significantly different from the scores at 1 and 2 s (which are equivalent) according to ANOVA followed by multiple comparisons. Performance between trial types was compared by proportion correct, because DI is not applicable to trials with no nonmatch stimuli (and thus no possible FA response). In this control task, the ISI (0.5, 1, 2, or 3 s) was fixed within daily sessions and randomly interleaved across 40 sessions, 10 at each ISI. Median number of trials per ISI was 919 for monkey F (black) and 727 for monkey S (gray). Each point on the curves for one intervening nonmatch is offset from a whole-number delay by 0.3 s to account for the added delay due to the presentation of that 0.3-s nonmatch stimulus.
Fig. 3.
Fig. 3.
Performance across sample categories (DI, mean + SE across sessions) for monkeys S and F (black and gray bars, respectively). Performance varied significantly as a function of category and animal, with a significant interaction effect (two-way ANOVA, all effects P < 10−4). Sound categories are BPN, PT, FM, TORC, Mvoc, other species’ vocalizations (voc), and environmental sounds (env). Categories have been sorted left to right by average performance across the two animals. Multiple-comparisons ANOVA identified performance for BPN, PT, and FM (grouped by the left bracket) as statistically equivalent, and better than performance for all other categories (grouped by the right bracket). We have distinguished these groups as “temporally simple” and “temporally complex.” TORCs were excluded from the one-way ANOVA because performance for this category clearly differed between subjects: TORCs were remembered well by monkey S but poorly by monkey F. The entire set of stimuli is illustrated in Fig. S1.
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References

    1. Baddeley A. Working memory: Looking back and looking forward. Nat Rev Neurosci. 2003;4:829–839. - PubMed
    1. Miller GA, Galanter E, Pribram KH. Plans and the Structure of Behavior. New York: Holt, Rinehard & Winston; 1960.
    1. Pasternak T, Greenlee MW. Working memory in primate sensory systems. Nat Rev Neurosci. 2005;6:97–107. - PubMed
    1. Cowan N. What are the differences between long-term, short-term, and working memory? Prog Brain Res. 2008;169:323–338. - PMC - PubMed
    1. Cowan N. Evolving conceptions of memory storage, selective attention, and their mutual constraints within the human information-processing system. Psychol Bull. 1988;104:163–191. - PubMed

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