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

Abstract

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...

Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys

“…Unlike the present study, no data from rats were reported to indicate whether the response deadline procedure actually succeeded in speeding the rats' responding, or whether rats responded at the same pace and the deadline effectively "threw out" all trials that would have taken longer. 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).…”

Two processes support visual recognition memory in rhesus monkeys

“…Another possible explanation of the difference is that we obtained ROCs by manipulating the monkeys' bias through differential reward payoffs in a block design using a running-recognition task, whereas in humans, ROCs are typically obtained by asking subjects, in a study/test design, to rate their recognition confidence on a continuous scale; however, several arguments speak against this explanation. First, a recent study in humans showed that ROCs obtained using a bias method are comparable in shape to ROCs obtained using the confidence method (14). Second, our control experiment suggests that the running recognition task in conjunction with differential reward payoffs did not influence accuracy differentially for the different bias levels.…”

Criterion noise in ratings-based recognition: Evidence from the effects of response scale length on recognition accuracy.

“…Some have argued that the inclusion of ratings so perverts the shape of the isosensitivity function that the broad consensus that evidence is graded rather than thresholded is wrong (Bröder & Schütz, 2009). However, there is compelling evidence that isosensitivity functions are in fact curvilinear even when estimated from manipulations of bias (Dube & Rotello, 2012; Koen & Yonelinas, 2011), indicating that the assumption of graded evidence is indeed correct. However, the exact shape of isosensitivity functions estimated from ratings does differ across conditions of differential bias (Van Zandt, 2000), so there is reason for concern that the underlying information available to the recognizer might not be equivalent in the two cases.…”