Cognitive mechanisms of memory for order in rhesus monkeys (Macaca mulatta)

One important aspect of episodic memory is the ability to remember the order in which events occurred. Memory for sequences in rats and has been shown to rely on the hippocampus and medial prefrontal cortex (DeVito and Eichenbaum (2011) J Neuro 31:3169-3175; Fortin et al. (2002) Nat Neuro 5:458-462). Rats with hippocampal lesions were impaired in selecting the odor that had appeared earlier in a sequence of five odors but were not impaired in recognition of previously sampled odors (Fortin et al., 2002; Kesner et al. (2002) Behav Neuro 116:286-290). These results suggest that order is not represented by relative familiarity or memory strength. However, the cognitive mechanisms underlying memory for order have not been determined. We presented monkeys with lists of five images drawn randomly from a pool of 6,000 images. At test, two images were presented and monkeys were rewarded for selecting the image that had appeared earlier in the studied list. Monkeys learned to discriminate the order of the images, even those that were consecutive in the studied list. In subsequent experiments, we found that discrimination of order was not controlled by list position or relative memory strength. Instead, monkeys used temporal order, a mechanism that appears to encode order of occurrence relative to other events, rather than in absolute time. We found that number of intervening images, rather than passage of time per se, most strongly determined the discriminability of order of occurrence. Better specifying the cognitive mechanisms nonhuman primates use to remember the order of events enhances this animal model of episodic memory, and may further inform our understanding of the functions of the hippocampus.