Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys

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.

[1]  G. Mandler Recognizing: The judgment of previous occurrence. , 1980 .

[2]  Tim Curran,et al.  Retrieval dynamics of recognition and frequency judgments: Evidence for separate processes of familiarity and recall. , 1994 .

[3]  A. Yonelinas,et al.  From humans to rats and back again: bridging the divide between human and animal studies of recognition memory with receiver operating characteristics. , 2011, Learning & memory.

[4]  L. Jacoby,et al.  Dissociations of processes in recognition memory: effects of interference and of response speed. , 1994, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[5]  E. Heit,et al.  Associative Recognition: a Case of Recall-to-reject Processing , 2022 .

[6]  L. Connors,et al.  The Washington Post , 2003 .

[7]  D. Schacter,et al.  The Evolution of Multiple Memory Systems , 1987 .

[8]  B. Dosher Discriminating preexperimental (semantic) from learned (episodic) associations: A speed-accuracy study , 1984, Cognitive Psychology.

[9]  David A. Caulton,et al.  Retrieval dynamics in recognition and list discrimination: Further evidence of separate processes of familiarity and recall , 1998, Memory & cognition.

[10]  R. Hampton,et al.  Monkeys Recall and Reproduce Simple Shapes from Memory , 2011, Current Biology.

[11]  M. Mishkin,et al.  Two processes support visual recognition memory in rhesus monkeys , 2011, Proceedings of the National Academy of Sciences.

[12]  Colleen M. Parks,et al.  Receiver operating characteristics (ROCs) in recognition memory: a review. , 2007, Psychological bulletin.

[13]  A. Yonelinas Receiver-operating characteristics in recognition memory: evidence for a dual-process model. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[14]  J. Wixted Dual-process theory and signal-detection theory of recognition memory. , 2007, Psychological review.

[15]  R. Hampton,et al.  Rhesus monkeys (Macaca mulatta) show robust primacy and recency in memory for lists from small, but not large, image sets , 2010, Behavioural Processes.

[16]  A. Yonelinas The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[17]  M Mishkin,et al.  An analysis of short-term visual memory in the monkey. , 1975, Journal of experimental psychology. Animal behavior processes.

[18]  H. Eichenbaum,et al.  Recognition memory: adding a response deadline eliminates recollection but spares familiarity. , 2010, Learning & memory.

[19]  L. Jacoby A process dissociation framework: Separating automatic from intentional uses of memory , 1991 .

[20]  H. Eichenbaum,et al.  Recollection-like memory retrieval in rats is dependent on the hippocampus , 2004, Nature.

[21]  L. Squire,et al.  Constructing receiver operating characteristics (ROCs) with experimental animals: cautionary notes. , 2008, Learning & memory.

[22]  M. Mishkin,et al.  Age differences in recognition memory of the rhesus monkey (Macaca mulatta) , 1987, Neurobiology of Aging.

[23]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[24]  Caren M. Rotello,et al.  Recall-to-Reject in Recognition: Evidence from ROC Curves ☆ ☆☆ , 2000 .

[25]  John T Wixted,et al.  Recollection can be weak and familiarity can be strong. , 2012, Journal of experimental psychology. Learning, memory, and cognition.