Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys

Abstract

One influential model of recognition posits two underlying memory processes: recollection, which is detailed but relatively slow, and familiarity, which is quick but lacks detail. Most of the evidence for this dual-process model in nonhumans has come from analyses of receiver operating characteristic (ROC) curves in rats, but whether ROC analyses can demonstrate dual processes has been repeatedly challenged. Here, we present independent converging evidence for the dual-process model from analyses of recognition errors made by rhesus monkeys. Recognition choices were made in three different ways depending on processing duration. Short-latency errors were disproportionately false alarms to familiar lures, suggesting control by familiarity. Medium-latency responses were less likely to be false alarms and were more accurate, suggesting onset of a recollective process that could correctly reject familiar lures. Long-latency responses were guesses. A response deadline increased false alarms, suggesting that limiting processing time weakened the contribution of recollection and strengthened the contribution of familiarity. Together, these findings suggest fast familiarity and slow recollection in monkeys, that monkeys use a "recollect to reject" strategy to countermand false familiarity, and that primate recognition performance is well-characterized by a dual-process model consisting of recollection and familiarity.

Nonnavigational spatial memory performance is unaffected by hippocampal damage in monkeys

“…Monkeys received full food rations after each day's testing, and water was available ad lib. All monkeys had prior experience with touchscreen‐based cognitive tasks (Basile & Hampton, , , , , , ; Gazes et al, ; Templer & Hampton, ). All procedures complied with US law and the National Institutes of Health guide for the care and use of laboratory animals.…”

Neurocognitive Aging and the Hippocampus across Species

“…However, little work has been done to determine whether aging alters recollection vs. familiarity processes in non-human primates. Recent studies using visual recognition memory tasks in rhesus monkeys suggest that performance is supported by recollection- and familiarity-like processes [24,25]. This opens up the possibility of using tasks that are highly analogous to the ones used in humans to study these memory processes in aged non-human primates.…”

Dissociation of dorso-lateral and dorso-medial prefrontal cortex contributions to familiarity and recollective processes in primates

“…The task is a variant of the well established delayed-matching-to-sample (i.e. recognitionmemory) paradigm in which a stimulus in a sample phase has to be judged as familiar or not in a subsequent choice phase after a short delay; the form of the task used is similar to that used by Basile and Hampton (2013) in that in the choice phase, to allow separation of hits, misses, false alarms, and correct rejections, one choice image is presented with one nonmatch button (black circle) such that the animal selects the choice image if it considers the choice image a match and selects black circle if it considers it is a non-match (see Fig.1A). In each trial, the animal initiated the task by holding the key-touch when cued to do so by a small red circular keytouch cue (located towards upper centre of screen; Fig.…”

“…the black circle) if the test-item was a non-match (these we refer to an 'nonmatch trials'). After a correct response, the intertrial interval was 3 s. However, following any error trial (including both incorrect response and aborted trials), the intertrial interval was 10 s Accordingly, on match trials the animal could either make a correct response ('hit') or an incorrect response ('miss') whereas on non-match trials the animal could either make a correct response ('correct rejection') or an incorrect response ('false alarm'); in this way the paradigm is similar to one previously used by Basile and Hampton (2013) but a key difference is that we did not restrict the stimulus set to just two stimuli as we used larger sets moreover we also varied the degree to which stimuli were either familiar or novel in the session. Specifically, in any given session 50% of the trials used trial-unique stimuli and 50% were 'repeat' stimuli used previously in the session (but not used in any previous session); in each session there were six repeat stimuli sorted into 3 pairs such that in each trial with repeat stimuli one pair was chosen at random and one member of the pair was randomly chosen to be the sample.…”