Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval
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Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval R. N. A. Henson, M. D. Rugg, and T. Shallice University College London Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/12/6/913/1758859/08989290051137468.pdf by guest on 18 May 2021 R. J. Dolan University College London and Royal Free Hospital School of Medicine, London Abstract & We used event-related functional magnetic resonance correct high-confidence judgements. Several regions, includ- imaging (efMRI) to investigate brain regions showing ing the precuneus, posterior cingulate, and left lateral differential responses as a function of confidence in an parietal cortex, showed greater responses to correct old episodic word recognition task. Twelve healthy volunteers than correct new judgements. The anterior left and right indicated whether their old±new judgments were made with prefrontal regions also showed an old±new difference, but high or low confidence. Hemodynamic responses associated for these regions the difference emerged relatively later in with each judgment were modeled with an ``early'' and a time. These results further support the proposal that ``late'' response function. As predicted by the monitoring different subregions of the prefrontal cortex subserve hypothesis generated from a previous recognition study different functions during episodic retrieval. These functions [Henson, R. N. A., Rugg, M. D., Shallice, T., Josephs, O., & are discussed in relation to a monitoring process, which Dolan, R. J. (1999a). Recollection and familiarity in recogni- operates when familiarity levels are close to response tion memory: An event-related fMRIstudy. Journal of criterion and is associated with nonconfident judgements, Neuroscience, 19, 3962±3972], a right dorsolateral prefrontal and a recollective process, which is associated with the region showed a greater response to correct low- versus confident recognition of old words. & INTRODUCTION magnetic resonance imaging (efMRI; Dale & Buckner, Numerous imaging studies have demonstrated activa- 1997; Josephs, Turner, & Friston, 1997; Zarahn, Aguirre, tion of the right prefrontal cortex during episodic mem- & D'Esposito, 1997), which permits responses to be ory retrieval (for reviews see Buckner & Koutstaal, 1998; conditionalized on both the subjective and objective Fletcher, Frith, & Rugg, 1997), and several different properties of individual trials, offers some resolution to hypotheses have been advanced concerning the func- this problem. In the present study, we used efMRI in an tional role of these activations. These hypotheses in- attempt to tease apart the neural correlates of retrieval clude the adoption of a retrieval mode (Kapur, Craik, success and retrieval monitoring by asking participants Brown, Houle, & Tulving, 1995), expenditure of retrieval to indicate the confidence of each of their old±new effort (Schacter, Alpert, Savage, Rauch, & Albert, 1996), judgements during a word recognition task. We propose probability of successful retrieval (Rugg, Fletcher, Frith, that increases in regional activity associated with correct Frackowiak, & Dolan, 1996), and monitoring the pro- old versus correct new judgements reflect the conse- ducts of retrieval cueing (Shallice et al., 1994). In many quences of retrieval success, whereas increases asso- situations, however, particularly in the blocked designs ciated with correct low- versus correct high-confidence adopted by the majority of these studies, the predictions judgements reflect the consequences of retrieval mon- of several of these hypotheses are confounded. In itoring. blocked studies that have manipulated the ratio of old This proposal is based on the findings of a pre- to new words for example (e.g., Rugg et al., 1996; vious efMRIstudy (Henson, Rugg, Shallice, Josephs, & Nyberg et al., 1995), the degree of retrieval success Dolan, 1999a), in which we attempted to identify and amount of retrieval monitoring are likely to be regions associated with the recollective experience highly correlated. The advent of event-related functional during recognition memory for words. Using the R/ D 2000 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 12:6, pp. 913±923 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/08989290051137468 by guest on 28 September 2021 K procedure of Tulving (1985), we observed greater Response Criterion responses associated with R than K judgements in several cortical regions, including the anterior pre- High Low Low High Confidence frontal cortex, lateral parietal cortex, and posterior ÒNewÓ ÒNewÓ ÒOldÓ ÒOldÓ Judgement cingulate. These regions were confined to the left hemisphere, however. The right dorsolateral prefron- tal cortex showed the opposite pattern of greater responses to K than R judgements. We hypothesized Old Words that this enhanced right dorsolateral prefrontal activ- New Words Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/12/6/913/1758859/08989290051137468.pdf by guest on 18 May 2021 ity reflected increased monitoring requirements when Probability recognition decisions were uncertain (as is likely, for example, when judgements are based on a feeling of familiarity in the absence of recollection). This hy- pothesis is an extension of the concept of retrieval monitoring developed by Koriat and Goldsmith ÒMemory StrengthÓ (1996) and Norman and Bobrow (1979), and incor- porated into the retrieval model of Burgess and Shallice (1996) as part of the ``memory editor'' Figure 1. Schematic depiction of signal detection models of process. In the context of a yes/no recognition task, recognition judgements. monitoring would include the examination of the products of memory retrieval (e.g., ``is the retrieved information relevant?'') and decision processes perti- for both single and dual process models we would still nent to the final judgment (e.g., ``is the information expect greater monitoring when memory strengths (or sufficient for me to respond yes?''). familiarity levels) are close to the old±new response In terms of signal detection models of recognition criterion. (e.g., Green & Swets, 1966; Murdock, 1965), decisions We predicted therefore that the right dorsolateral are uncertain when memory strength is close to the prefrontal cortex (BA 9/46) would show greater re- response criterion. These models represent old and new sponses associated with low- than high-confidence items as overlapping distributions of ``memory judgements, regardless of whether the word was old strength'', upon which participants impose a criterion or new. We were also interested in the response for making ``old'' versus ``new'' judgements (Figure 1). characteristics of other right prefrontal regions impli- Judgements to items with strengths far from the re- cated in previous studies, such as the anterior (BA 10) sponse criterion (old or new) are made with high and ventral (BA 45/47) prefrontal cortex, which might confidence, whereas judgements to items close to the show different response patterns, on the hypothesis response criterion are made with low confidence. Be- that the right prefrontal cortex comprises several func- cause memory strength is a continuum, these models tionally dissociable subregions (Henson, Shallice, & illustrate that retrieval monitoring is not necessarily Dolan, 1999b). contingent on retrieval ``success'', as operationally de- fined by a correct ``old'' judgement. Rather, memory RESULTS strength can be regarded as evidential, comprising many types of information retrieved in response to a recogni- Behavioral Data tion cue, which require monitoring for their validity and The mean proportions and reaction times for correct appropriateness. judgements to old and new words are shown in Table Other models assume that more than one process 1. Collapsing across confidence, overall memory per- underlies recognition memory (e.g., Jacoby, 1996; formance was good, as indexed by a Hit RateÀFalse Mandler, 1980). The dual-process model of Atkinson Alarm rate of 0.91À0.17 = 0.74. The proportions of and Juola (1974), for example, assumes that items correct new judgements made with low and high with moderate levels of memory strength are sub- confidence were approximately equal, whereas a jected to a further set of retrieval operations. The greater proportion of correct old judgements were dual-process model of Yonelinas, Dobbins, Szymanski, made with high than low confidence, as confirmed by Dhaliwal and King (1996), on the other hand, assumes a significant interaction in a two-way ANOVA, F(1,11) independent contributions of recollection and famil- = 31.17, p < .001. A two-way ANOVA on median iarity. Recollection is formalized as an all-or-none, correct reaction times showed significantly longer RTs threshold phenomenon (which would be associated for low- versus high-confidence judgements, F(1,11) = with high-confidence old judgments). Familiarity, how- 10.3, p < .01, and for new versus old judgements, ever, is formalized as a continuous quantity, equivalent F(1,11) = 9.42, p < .05, though the old±new differ- to memory strength in signal detection models. Thus, ence was greater for confident old judgements, as 914 Journal of Cognitive Neuroscience Volume 12, Number 6 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/08989290051137468 by guest on 28 September 2021 Table 1. Proportions of Old and New Words and Reaction sponses might be delayed and/or prolonged in time, as Times (RT) for Correct High- and Low-Confidence