Similar time course of fast familiarity and slow recollection processes for recognition memory in humans and macaques

Abstract

According to dual-process theory, recognition memory performance draws upon two processes, familiarity and recollection. The relative contribution to recognition memory are commonly distinguished in humans by analyzing receiveroperating-characteristics (ROC) curves; analogous methods are more complex and very rare in animals but fast familiarity and slow recollective-like processes (FF/SR) have been detected in nonhuman primates (NHPs) based on analyzing recognition error response time profiles. The relative utility of these methods to investigate familiarity and recollection/recollection-like processes across species is uncertain; indeed, even how comparable the FF/SR measures are across humans and NHPs remains unclear. Therefore, in this study a broadly similar recognition memory task was exploited in both humans and a NHP to investigate the time course of the two recognition processes. We first show that the FF/SR dissociation exists in this task in human participants and then we demonstrate a similar profile in the NHP which suggests that FF/SR processes are comparable across species. We then verified, using ROC-derived indices for each time-bin in the FF/SR profile, that the ROC and FF/SR measures are related. Hence, we argue that the FF/SR approach, procedurally easier in nonhuman animals, can be used as a decent proxy to investigate these two recognition processes in future animal studies, important given that scant data exists as to the neural basis underlying recollection yet many of the most informative techniques primarily exist in animal models.

Low‐beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task‐related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity

“…The task is a variant of the well-established delayed matching-to-sample recognition memory paradigm in which an object 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 we used is similar in broad terms to that used by Basile and Hampton (2013) and very similar indeed to the version we created and used in an earlier study (Wu et al, 2020). In all these tasks, a key task design feature is that in the choice phase, to allow separation of hits, misses, false alarms, and correct rejections, one choice stimulus is presented along with one nonmatch button (black circle) such that the animals have a binary choice.…”

“…This is the reason that response time was not involved in our analyses in this study. However, our previous behavioural study analysed response times in detail in a close variant of the same task (Wu et al, 2020). The object stimulus in the choice stage was either the identical stimulus to the sample seen earlier in the trial, or it was not identical to the sample.…”

“…For example, high‐beta frequency rTMS over frontal eye fields (an area of human PFC) enhances perceptual discrimination, whereas response criterion is lowered by delivery of rTMS over the same region at a gamma frequency (Chanes et al, 2013). As for the choice of a working memory/short‐term recognition memory task suitable for both primate species, we opted for a well validated task (Wu et al, 2020), itself based on a paradigm introduced by Basile and Hampton (2013). This task has established variants for NHPs and humans that differ to a degree but nonetheless elicit broadly similar performance profiles in human and macaques (Wu et al, 2020).…”

“…As for the choice of a working memory/short‐term recognition memory task suitable for both primate species, we opted for a well validated task (Wu et al, 2020), itself based on a paradigm introduced by Basile and Hampton (2013). This task has established variants for NHPs and humans that differ to a degree but nonetheless elicit broadly similar performance profiles in human and macaques (Wu et al, 2020). Specifically, both species show corresponding profiles of so‐called fast familiarity (FF) and slow recollection (SR) responses.…”

“…Specifically, both species show corresponding profiles of so‐called fast familiarity (FF) and slow recollection (SR) responses. Moreover, Wu et al (2020) validated these FF/SR profiles against ROC‐based dual‐process model fitting. That said, debate remains as to whether animals also provide suitable models of recollection (e.g., see Eichenbaum et al, 2005, 2008; Wixted & Squire (2008)), although it has been shown, using ROC procedures and dual‐process models similar to those in humans, that processes akin to recollection exist in macaques (Guderian et al, 2011).…”