Recognition memory: Adding a response deadline eliminates recollection but spares familiarity

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.

Section: Discussionsupporting

confidence: 82%

Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys

Basile

Hampton

2013

“…A further limitation is that it is difficult with animals to isolate those cognitive processes that might contribute to explicit human recognition memory, i.e., familiarity and recollection. Even so, important behavioral advances have been achieved in trying to separate these processes in rats (Sauvage et al 2008(Sauvage et al , 2010, though they have yet to be applied to the diencephalon.…”

Section: Findings From Animal Studiesmentioning

confidence: 99%

Unraveling the contributions of the diencephalon to recognition memory: A review

Aggleton¹,

Dumont²,

Warburton³

2011

138

111

Both clinical investigations and studies with animals reveal nuclei within the diencephalon that are vital for recognition memory (the judgment of prior occurrence). This review seeks to identify these nuclei and to consider why they might be important for recognition memory. Despite the lack of clinical cases with circumscribed pathology within the diencephalon and apparent species differences, convergent evidence from a variety of sources implicates a subgroup of medial diencephalic nuclei. It is supposed that the key functional interactions of this subgroup of diencephalic nuclei are with the medial temporal lobe, the prefrontal cortex, and with cingulate regions. In addition, some of the clinical evidence most readily supports dual-process models of recognition, which assume two independent cognitive processes (recollective-based and familiarity-based) that combine to direct recognition judgments. From this array of information a "multi-effect multinuclei" model is proposed, in which the mammillary bodies and the anterior thalamic nuclei are of preeminent importance for recollective-based recognition. The medial dorsal thalamic nucleus is thought to contribute to familiarity-based recognition, but this nucleus, along with various midline and intralaminar thalamic nuclei, is also assumed to have broader, indirect effects upon both recollective-based and familiarity-based recognition.Clinical studies repeatedly show that diencephalic pathology can impair recognition memory. Even so, there is no agreed locus within the diencephalon responsible for this memory loss and, hence, no agreed mechanism to explain the impairment. The present review examines both clinical and animal findings, and from this information a multi-effect multi-nuclei (MEMN) model emerges to explain the contributions of the diencephalon to recognition memory.At the outset, it is necessary to refine the focus of this review and to define some of its principal terms. The diencephalon comprises the thalamus and hypothalamus but, as will be explained, only the more medial parts of the diencephalon will be considered in detail. Recognition memory refers to the ability to detect whether a stimulus (e.g., a word, face, picture, object, or sound) has previously been encountered. As a consequence, this review is not about item identification (sometimes also confusingly referred to as recognition). Likewise, conditions that have broad disruptive effects on cognition, e.g., dementia, will not be considered even though recognition is typically impaired. Distinctions will be made between "item recognition," where the task is to determine if an individual item is novel or familiar, and "associative recognition," where all the individual items being experienced are familiar, but their particular combination is novel. A further, distinct ability is "recency" discrimination-the ability to determine which of two familiar stimuli has been experienced more recently. Both studies of amnesia and electrophysiological recordings show how recency memory and recogniti...

“…2 Based on the results of Sauvage et al (2010), we expected that speeding responses would lead to a decrease in overall recognition performance, and that this decrease would arise because of a decrease in recollection but not in familiarity.…”

mentioning

confidence: 99%

“…Overall recognition Figure 1. Aggregate ROCs (left) and average estimates of recollection and familiarity (right) for rats from Sauvage et al (2010) and humans in the present experiment. (A,B) Estimates of recollection and familiarity derived from recognition ROCs in rats from Sauvage et al (2010) demonstrated that speeding responses selectively reduced the contribution of recollection, but not familiarity, to recognition memory ( * P , 0.05).…”

mentioning

confidence: 99%

“…Aggregate ROCs (left) and average estimates of recollection and familiarity (right) for rats from Sauvage et al (2010) and humans in the present experiment. (A,B) Estimates of recollection and familiarity derived from recognition ROCs in rats from Sauvage et al (2010) demonstrated that speeding responses selectively reduced the contribution of recollection, but not familiarity, to recognition memory ( * P , 0.05). (C,D) The results from the current experiment using a confidence bias procedure replicate the findings of Sauvage et al (2010) by showing that estimates of recollection were significantly reduced for participants in the speeded condition (N ¼ 23) compared to participants in the selfpaced condition (N ¼ 20), whereas estimates of familiarity remained unchanged.…”

mentioning

confidence: 99%

See 1 more Smart Citation

From humans to rats and back again: Bridging the divide between human and animal studies of recognition memory with receiver operating characteristics

Koen

Yonelinas²

2011

Receiver operating characteristics (ROCs) have been used extensively to study the processes underlying human recognition memory, and this method has recently been applied in studies of rats. However, the extent to which the results from human and animal studies converge is neither entirely clear, nor is it known how the different methods used to obtain ROCs in different species impact the results. A recent study used a response bias ROC manipulation with rats and demonstrated that speeding memory responses reduced the contribution of recollection, not familiarity. The current study confirms this finding in humans using a comparable response bias method. Moreover, a comparison of the response bias methods commonly used in animal studies and the confidence rating method typically employed in human studies produced similar ROC functions. The present results suggest that the analysis of recognition memory ROCs provides a fruitful method to bridge the human and animal memory literatures. [Supplemental material is available for this article.]It is well established that recognition memory can be based on recollection of qualitative details about the study episode or on assessments of familiarity (Mandler 1980;Jacoby 1991;Yonelinas 2002;Yonelinas et al. 2010). Evidence for this distinction comes from studies of human participants, as well as studies of rats and nonhuman primates (Aggleton and Brown 2006;Eichenbaum et al. 2007). However, a full integration of the human and animal literatures has been limited because the paradigms typically used in studies of humans to examine these processes are not suitable for other species. For example, recollection is often indexed in humans using verbal free recall paradigms or on the basis of subjective report methods where individuals indicate when recognition is accompanied by conscious recollection or only by feelings of familiarity (Mandler 1980;Tulving 1985).One method that holds some promise in bridging the human and animal literatures is the analysis of receiver operating characteristics (ROCs) (Macmillan and Creelman 2005). This approach involves examining recognition memory across different levels of response bias (i.e., the probability of endorsing an item as previously studied) and can be used to extract estimates of recollection and familiarity (Yonelinas 2001;Yonelinas and Parks 2007). The method has been used quite extensively in the human literature, and has been found to lead to conclusions that converge with those based on other measurement methods such as free recall and subjective reports (for review, see Yonelinas 2002).Recently, the ROC methodology has been applied to study recognition memory in rats (for review, see Eichenbaum et al. 2010;Sauvage 2010). For example, hippocampal lesions have been found to selectively impair recollection-based recognition, but do not impact familiarity-based recognition (Fortin et al. 2004;Sauvage et al. 2008). These results are consistent with ROC studies in humans, which have also shown that hippocampal damage disrupts recolle...