Elsevier

NeuroImage

Volume 29, Issue 4, 15 February 2006, Pages 1150-1160
NeuroImage

Rapid Communication
Understanding metamemory: Neural correlates of the cognitive process and subjective level of confidence in recognition memory

https://doi.org/10.1016/j.neuroimage.2005.09.058Get rights and content

Abstract

An essential feature of human memory is the capacity to assess confidence in one's own memory performance, but the neural mechanisms underlying the process of determining confidence in memory performance have not yet been isolated. Using functional magnetic resonance imaging, we examined both the process of confidence assessment and the subjective level of high or low confidence expressed during this process. The comparison of confidence assessment to recognition showed greater relative activation during confidence assessment in medial and lateral parietal regions, which typically deactivate during cognitive tasks, previously described as part of the “default network”. Furthermore, comparisons of high versus low confidence judgments revealed modulation of neural activity in the hippocampus, cingulate and other limbic regions, previously described as the Circuit of Papez. Our findings suggest that activity in two distinct networks of brain regions contribute to the subjective experience of “knowing you know” through memory monitoring processes and signaling subjective confidence level for recognition memory.

Introduction

The ability to accurately evaluate one's own memory performance is a critical feature of normal memory function. Confidence judgments are one commonly used method for determining an individual's belief that the information retrieved from memory is accurate. The degree of confidence that an individual expresses in a memory plays a critical role in how an outsider evaluates the verity of that memory (Wells et al., 2002). Furthermore, functional magnetic resonance imaging (fMRI) studies of encoding (Kirchhoff et al., 2000, Sperling et al., 2003, Wagner et al., 1998) and retrieval (Eldridge et al., 2000, Henson et al., 1999a, Henson et al., 2000) have used a combination of subjective confidence and objective accuracy to define successful memory. Despite the common use of subjective confidence judgments, surprisingly, little is known about the neural mechanisms underlying confidence assessment and other metamemory processes engaged in “knowing you know.”

Confidence judgments involve both the cognitive process of confidence assessment and the subjective feeling of confidence. One common use of confidence judgments in studies of recognition memory assumes that it reflects memory strength, especially in studies that use signal detection theory and receiver-operating characteristics (ROC) (Yonelinas, 1994). However, the use of confidence ratings in these procedures has been questioned on a theoretical level because it assumes that the classifier maintains an ordered set of criteria, which may not be the case (Malmberg, 2002). Moreover, laboratory manipulations have shown behavioral dissociations between confidence and accuracy (Brewer et al., 2002, Busey et al., 2000, Shaw and Zerr, 2003), suggesting that they may not be based on entirely the same information. In addition to the strength of the memory trace, it has been hypothesized that confidence ratings also may rely on ease of retrieval, retrieval fluency, ease of processing the retrieval cue, and also heuristics about the study and test conditions and heuristics about a subject's own memory (Busey et al., 2000). Some or all of these factors may contribute to the subjective level of confidence that a subject experiences for a given memory, and thus, high and low confidence decisions might differ on these dimensions. Furthermore, the cognitive processes underlying confidence assessment requires subjects to introspectively consider these factors. Thus, confidence in recognition memory may be based on factors other than memory strength and may differ from simple recognition tasks.

Although research to date has not isolated the cognitive process of confidence assessment from the subjective feeling of confidence, several studies have investigated other subjective aspects of memory. Using a procedure in which subjects indicated during retrieval whether they specifically recollect an item (“remember”) or whether it just seems familiar (“know”), greater activity for correct “remember” trials compared to correct “know” trials has been shown in left prefrontal, left lateral parietal, and posterior cingulate regions (Eldridge et al., 2000, Henson et al., 1999a), and also in the medial temporal lobe (MTL) (Eldridge et al., 2000). In contrast, the right prefrontal cortex and anterior cingulate showed greater activity for correct “know” compared to correct “remember” trials (Eldridge et al., 2000, Henson et al., 1999a). Using confidence judgments, Henson et al. (2000) showed greater activity in the right prefrontal cortex for low confidence correct trials compared with high confidence correct trials. Another recent study examined recollection and familiarity using confidence ratings and showed that anterior prefrontal, medial, and lateral parietal regions modulated based on familiarity confidence, and that medial prefrontal, medial parietal, and medial temporal regions distinguished recollection and familiarity (Yonelinas et al., 2005). These studies reported neural differences based on subjective aspects of memory, but the paradigms that were used did not allow a distinction between the processes involved in subjective assessment of one's own memory on the one hand, and retrieval processes on the other because, in these studies, the subject's behavioral response included both subjective and objective aspects of memory. Further work that isolates the different contributions of memory monitoring and subjective experience of memory is needed in order to better elucidate the contributing mechanisms to “knowing you know”.

In this study, we report the specific neural mechanisms supporting confidence assessment as distinct from recognition judgments, and the neural correlates of high and low confidence, respectively. We used a well-characterized face–name associative paradigm, for which we have previously reported two findings during encoding related to subsequent subjective confidence level (Chua et al., 2004, Sperling et al., 2003). We undertook the present study to examine the neural correlates of confidence in recognition memory during recognition and confidence assessment. We scanned during encoding, recognition, and a post-recognition confidence assessment task. This design allows us to investigate the pattern of activation associated with the underlying cognitive processes of confidence assessment as compared with those underlying recognition. We also investigated the neural mechanisms associated with the subjective level confidence by comparing activation during high versus low confidence trials.

Section snippets

Subjects

Twenty right-handed, healthy young subjects (ages 20–33, 10 F/10 M) participated in this study. All subjects were free from psychiatric and neurologic illness, and none were taking medications with known central nervous system effects. All subjects were screened for contraindications to MRI. Each subject provided written informed consent in a manner approved by the Human Research Committee at Massachusetts General Hospital, Boston, MA.

For two of the 20 subjects, only partial data were collected

Behavioral results

During the recognition/confidence phase, subjects correctly chose the name identified with the face with high confidence (HC-Correct) for 65.9 ± 13.9% of the trials, and each subject performed above the chance rate of 33%. For the face–name pairs on the recognition test, the majority of responses were HC-Correct (78 ± 20 trials), with fewer HC-Incorrect (6 ± 4), LC-Correct (14 ± 9), and LC-Incorrect (16 ± 9) response types.

During recognition, a repeated measures 2 × 2 factorial ANOVA revealed

Discussion

In this study, we isolated the neural mechanisms supporting two distinct components of confidence judgments: (1) the process of confidence assessment and (2) the subjective level of confidence expressed. We examined the process of confidence assessment by comparing recognition trials to confidence assessment trials holding behavioral response constant, and we examined the level of confidence by comparing high to low confidence trials during confidence assessment. Medial and lateral parietal

Acknowledgments

We would like to thank Mary Foley and Larry White for their help with scan acquisition. This work was supported by NINDS: K23-NS02189 (RS); NIA: P01-AG-04953 (RS); the AFAR Beeson Scholars in Aging Program (RS); NIMH: MH60941 (DS); NIA: R01-AG08441 (DS); NCRR: P41RR14075; the MIND Institute; the Anthinoula A. Martinos Center for Biomedical Imaging; and the Harvard Center for Neurodegeneration and Repair.

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