Two processes support visual recognition memory in rhesus monkeys

Abstract

A large body of evidence in humans suggests that recognition memory can be supported by both recollection and familiarity. Recollection-based recognition is characterized by the retrieval of contextual information about the episode in which an item was previously encountered, whereas familiarity-based recognition is characterized instead by knowledge only that the item had been encountered previously in the absence of any context. To date, it is unknown whether monkeys rely on similar mnemonic processes to perform recognition memory tasks. Here, we present evidence from the analysis of receiver operating characteristics, suggesting that visual recognition memory in rhesus monkeys also can be supported by two separate processes and that these processes have features considered to be characteristic of recollection and familiarity. Thus, the present study provides converging evidence across species for a dual process model of recognition memory and opens up the possibility of studying the neural mechanisms of recognition memory in nonhuman primates on tasks that are highly similar to the ones used in humans. I n humans, dual process models of recognition memory, although different in detail, share the core idea that both recollection and familiarity contribute to this mnemonic function (1-5). Recollection is characterized by the retrieval of contextual information about the episode in which an item was encountered, whereas familiarity lacks this context, relying solely on knowledge of prior occurrence. The possibility that nonhuman animals also use separable memory processes to solve recognition memory tasks has begun to be experimentally addressed (6-8), an important shift, inasmuch as an understanding of how the brain gives rise to different memory functions in various species is critical for relating molecular and cellular findings in animals to behavioral and neuroimaging research conducted in humans.Recollection and familiarity are commonly viewed as retrieval processes that support potentially independent routes of cognitive access to stored information. This distinction has been operationalized based on the analysis of receiver operating characteristics (ROCs) (5). ROCs in recognition memory relate the proportion of correctly recognized repeated or old items (hit rate) to the proportion of incorrectly recognized novel distracters (false alarm rate) as a function of response criterion (bias to respond "old"). In a typical recognition memory test aimed at characterizing ROCs, subjects would encounter a list of previously studied items intermixed with new items and be asked to rate how confidently they recognize each item on an arbitrary scale [e.g., ranging from one (sure that it is new) to six (sure that it is old), with two to five reflecting less confident judgments]. These confidence ratings represent different decision criteria, and an ROC curve is produced by plotting the hit rate against the corresponding false alarm rate as a function of decision criterion.Recognition memory ROCs in humans are typicall...

Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys

“…Similar results have also been found in humans using speeded recognition procedures and the same ROC estimates of recollection and familiarity (Koen and Yonelinas 2011). Finally, a recent study in monkeys has also found ROC curves that are curvilinear and asymmetrical under normal recognition conditions, suggesting that visual recognition in monkeys is also supported by recollection and familiarity (Guderian et al 2011). …”

“…Unlike standard recognition tests, in which the target stimulus is re-presented at test and can produce familiarity, the recall test requires monkeys to reproduce a remembered stimulus from memory, suggesting recollection. Second, receiver operating characteristic (ROC) curves for monkeys performing a recognition test are similar to those seen with humans when familiarity and recollection both contribute to performance (Guderian et al 2011). ROC curves plot correct recognition of targets and incorrect recognition of lures as a function of the subject's bias to report any stimulus as having been seen before (Yonelinas 1994).…”

“…ROC curves derived from tests of human recognition are curvilinear, which is diagnostic of familiarity, and asymmetrical, which is diagnostic of recollection (Yonelinas and Parks 2007). ROC curves derived from tests of monkey recognition are also curvilinear and asymmetrical (Guderian et al 2011), suggesting that both familiarity and recollection contribute to recognition in monkeys. Similar results have also been found for rats (Fortin et al 2004).…”

Mechanisms of Synaptic Plasticity and Recognition Memory in the Perirhinal Cortex

“…2,9,[16][17][18][19] In rats, these impairments are seen in tests of recognition memory that rely upon spontaneous preference for novel objects and for the purposes of this review, we will focus upon studies of novel object recognition memory.…”

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.…”