Animal memory: A review of delayed matching-to-sample data

Highlights

• We tested animal working memory using meta-analyses on delayed matching-to-sample data.

• Without delays we found no evidence for differences between mammals, birds and bees.

• We cannot exclude that birds match the performance exhibited by mammals.

• Neither monkeys nor apes stand out when it comes to memory performance.

• Animals use specialized and general memory systems for different kinds of information.

Abstract

We performed a meta-analysis of over 90 data sets from delayed matching-to-sample (DMTS) studies with 25 species (birds, mammals, and bees). In DMTS, a sample stimulus is first presented and then removed. After a delay, two (or more) comparison stimuli are presented, and the subject is rewarded for choosing the one matching the sample. We used data on performance vs. delay length to estimate two parameters informative of working memory abilities: the maximum performance possible with no delay (comparison stimuli presented as soon as the sample is removed), and the rate of performance decay as the delay is lengthened (related to memory span). We conclude that there is little evidence that zero-delay performance varies between these species. There is evidence that pigeons do not perform as well as mammals at longer delay intervals. Pigeons, however, are the only extensively studied bird, and we cannot exclude that other birds may be able to bridge as long a delay as mammals. Extensive training may improve memory, although the data are open to other interpretations. Overall, DMTS studies suggest memory spans ranging from a few seconds to several minutes. We suggest that observations of animals exhibiting much longer memory spans (days to months) can be explained in terms of specialized memory systems that deal with specific, biologically significant information, such as food caches. Events that do not trigger these systems, on the other hand, appear to be remembered for only a short time.

This article is part of a Special Issue entitled: In Honor of Jerry Hogan.

Introduction

Animal memory is the object of enduring fascination and debate (Suddendorf and Busby, 2003, Raby et al., 2007, Clayton and Dickinson, 1998, Roberts, 2002, Bouton, 2007, Pearce, 2013, Kendrick et al., 1986). Even a cursory look at the literature reveals that sometimes animals appear to remember events in detail, and for a long time, while sometimes they seem to forget surprisingly fast. For example, many jays (family Corvidae) can remember the location of hidden food for many months (Bossema, 1979, Bednekoff et al., 1997), but have difficulty remembering simple color stimuli for more than 25–40 s (Olson et al., 1995). This is just one example of the great variation in memory performance that has led scholars to widely different conclusions. Some maintain that non-human animals have no explicit memories of past events, that is, they cannot recollect them in the same way as we do when we think about, say, childhood vacations (Roberts, 2002, Suddendorf and Busby, 2003). Others, in contrast, conclude that we have evidence that animals have “episodic-like” memories perhaps not dissimilar from those of humans (Clayton et al., 2001a, Clayton et al., 2001, Zentall, 2005). Comparison with human memory is central to the debate about non-human memory. Humans, in fact, appear capable of remembering practically arbitrary events for very long times without appreciable decline in performance, notably in tasks in which most other species perform poorly (Overman and Doty, 1980).

Here we review well-controlled experiments using the delayed matching-to-sample paradigm (DMTS, summarized below), one of a number of tasks that has been used to probe animals’ working memory (Bouton, 2007, Pearce, 2013). By “working memory” we mean information about an event that is maintained for some time in the absence of reinforcement, and that can be used to guide behavior at a later time (Pribram et al., 1960, Baddeley, 1991). We are particularly interested in events without specific biological significance, such as colored lights, visual patterns, or sounds, as typically used in laboratory studies. We ask whether we can discern any species differences in working memory, and whether memory can be improved by training. We conclude by suggesting that animal memory is best characterized as the sum of specialized memory capacities, different across species and potentially lasting a long time, and a general memory capacity that works in essentially the same way in all non-human species, and which has a limited span ranging between a few seconds and a few minutes.