Elsevier

NeuroImage

Volume 26, Issue 3, 1 July 2005, Pages 932-940
NeuroImage

Functional network in the prefrontal cortex during episodic memory retrieval

https://doi.org/10.1016/j.neuroimage.2005.03.004Get rights and content

Abstract

A recent consistent finding in neuroimaging studies of human memory is that the prefrontal cortex (PFC) is activated during episodic memory retrieval. To date, however, there has been no direct evidence to explain how activity in the right and left PFC and in the anterior and posterior PFC are functionally interconnected. The goal of the present study was to obtain such evidence by event-related functional magnetic resonance imaging (MRI) and the functional connectivity method. Subjects were first asked to try to remember a series of associate-word lists outside the MRI scanner in preparation for a later recognition test. In the MRI scanning phase, they were asked to make recognition judgments in regard to old words, semantically related lure words, and unrelated new words. The analysis of functional connectivity revealed that the posterior PFC in each hemisphere had strong functional interconnections with the contralateral posterior PFC, whereas the anterior PFC in each hemisphere had only weak functional interconnections with the contralateral anterior PFC. No strong functional interconnections were found between the anterior and posterior PFC in either hemisphere. These findings support the hypothesis of an associative contribution of the bilateral posterior PFC to episodic memory retrieval and a dissociative contribution of the bilateral anterior PFC.

Introduction

A consistent finding in recent functional neuroimaging studies of human memory is that the lateral prefrontal cortex (PFC) is activated during episodic memory retrieval (Buckner and Wheeler, 2001, Cabeza and Nyberg, 2000, Fletcher and Henson, 2001, Rugg and Wilding, 2000). Some of the studies have shown the right and left PFC to have separate roles during episodic retrieval processes (for reviews, see Buckner and Wheeler, 2001, Fletcher and Henson, 2001, Ramnani and Owen, 2004), and several of them have indicated that the function of the right PFC is within the context of strategic attitudes during retrieval (Düzel et al., 1999, Kapur et al., 1995, Nyberg et al., 1995, Rugg and Wilding, 2000, Rugg et al., 2000, Schacter et al., 1996a), of products of retrieval (McDermott et al., 2000, Rugg et al., 1998, Wagner et al., 1998), and of evaluational monitoring processes during or after retrieval (Allan et al., 2000, Henson et al., 1999b, MacLeod et al., 1998, Rugg et al., 1999). The function of the left PFC, on the other hand, has been characterized as being strategic retrieval of source information (Ranganath and Paller, 1999, Ranganath et al., 2000, Rugg et al., 1999) and semantic processing (Poldrack et al., 1999). Although some of these findings are based on the laterality data of broader PFC activations that include the anterior and posterior regions, many of these findings are based on the data showing activations in the anterior regions of the PFC. Some comprehensive hypotheses that focus on the functional interrelation between the PFC regions have also been proposed. One hypothesis states that the right PFC subserves more heuristic (automatic) judgments based on easily assessed qualities, such as familiarity or perceptual detail, whereas the left PFC subserves more systematic judgments requiring more deliberative decisions (Johnson and Raye, 1998, Nolde et al., 1998a, Nolde et al., 1998b, Ranganath et al., 2000, Raye et al., 2000). Another hypothesis states that the right PFC is more involved in monitoring and verification, whereas the left PFC is more involved in the production of semantically guided information (Cabeza et al., 2003).

Other studies have shown the anterior ventrolateral and posterior dorsolateral PFC to have separate roles, and several hypotheses have been proposed to explain the functional interrelation between the anterior and posterior PFC. One hypothesis, based on the results of previous studies on cognitive control, states that the posterior PFC supports response selection, which implements context-dependent biasing or dynamic filtering (Banich et al., 2000, MacDonald et al., 2000, Miller and Cohen, 2001), or refreshing, which is required for reactivation of representations that were recently active but have subsequently begun to decay (Johnson et al., 2002, Johnson et al., 2003, Raye et al., 2002), whereas the anterior PFC supports managing subgoals and integrating representations during the course of ongoing processing (Badre and Wagner, 2004). Another hypothesis based on the results of studies on working memory states that the posterior PFC subserves the monitoring and manipulation of the representations held in material-independent working memory, whereas the anterior PFC subserves the maintenance and evaluation of representations held in material-specific working memory (Wagner, 1999). Yet, another hypothesis states that the posterior PFC is involved when externally generated information is being evaluated, whereas the anterior PFC becomes recruited when internally generated information needs to be evaluated (Christoff and Gabrieli, 2000).

Although these hypotheses describing the functional interrelations between the right and left PFC and between the anterior and posterior PFC have to some extent been supported by previous studies, there has been no direct evidence showing whether the functions of the four PFC regions (right anterior, left anterior, right posterior, and left posterior PFC) are completely dissociate or partly dissociate during episodic memory retrieval. Since the similarity and diversity have been postulated to exist among the processing components of episodic memory retrieval, the functions of four PFC regions may be partly dissociate. The functional connectivity method may be useful in answering these questions. It has often been used to identify the temporal coherence among neuronal activity in spatially distinct brain regions by applying imaging data obtained by fMRI and positron emission tomography (PET) (Büchel and Friston, 1998, Büchel et al., 1999, Friston, 1994, Friston et al., 1995c).

A previous study that focused on functional interconnections within the PFC network during memory retrieval showed that the right PFC regions (BA 9, 10, and 47) were positively associated during recall (Cabeza et al., 1997), and other studies have provided evidence of a functional differentiation of the right anterior PFC (BA 10) and right posterior PFC (BA 45/47) (McIntosh, 1999, McIntosh et al., 1997). Brain areas whose activity during recognition was found to be positively correlated with activity in the right anterior PFC included widespread areas of the PFC and inferior temporal cortex bilaterally (Grady et al., 2001). Although these findings regarding prefrontal interconnections are very helpful, the functional interconnections among the four PFC regions during episodic memory retrieval remain unclear.

In the present study, we used functional magnetic resonance imaging (fMRI) and the functional connectivity method to reveal the interconnections among the four PFC regions during episodic memory retrieval. To accomplish our purpose, we should use a task that requires subjects to employ all four PFC regions. We therefore used a revised version of the typical false recognition task referred to as the DRM paradigm originally created by Deese (1959) and Roediger and McDermott (1995). In previous neuroimaging studies, which used the original DRM paradigm, the bilateral anterior and posterior PFC regions and the medial temporal regions were activated during retrieval (Cabeza et al., 2001, Schacter et al., 1996b, Schacter et al., 1997). To ensure activation in all four PFC regions, we made the task more difficult by requiring subjects to make a recognition judgment in regard to words presented in pairs. This modification increases the possibility of involving all four PFC regions during performance of the task, because maintaining responses to paired words requires more complicated retrieval processes and higher working memory load. Evidence of strong functional connectivity between the right and left PFC would suggest that the two hemispheres function in collaboration. Weak or no connectivity between the right and left PFC would suggest that the two hemispheres function independently and would support their having separate roles. Moreover, if different functional connectivity patterns were found between the two hemispheres in the anterior and posterior PFC and weak or no connectivity between the anterior and posterior PFC, it would suggest that the functions of four PFC regions are partly dissociate.

Based on the results of the previous neuroimaging findings described above, we hypothesized an associative right–left functional interconnection in the posterior PFC (areas Y < 50 in the middle frontal gyrus) and a dissociative right–left functional interconnection in the anterior PFC (areas Y ≥ 50 in the middle frontal gyrus), and the hypothesis predicted that different right–left connectivity patterns would be found in the anterior and posterior PFC. To test it, we first compared activation patterns associated with three types of responses (hit, false alarm, and correct rejection), then conducted the time-course analyses of MR signals to identify the temporal characteristics of the patterns in specific PFC regions, and finally, examined the functional interconnections among those regions by means of a connectivity analysis.

Section snippets

Subjects

Thirteen healthy subjects (ten males and three females; average age 27.4 years; average years of education 16.3) were paid to participate in this study. Handedness was assessed by the Edinburgh Handedness Survey (Oldfield, 1971), and all subjects were right-handed. The fMRI experiments were conducted under a protocol approved by the Institutional Ethics Committee of the National Institute of Radiological Sciences of Japan. All of the subjects gave written informed consent prior to participation

Behavioral results

Even though they recognized many of the old words as old and correctly rejected many of the unrelated new words as new, the subjects tended to recognize both of the related lure words as old. The results are based on what the subjects actually responded, not based on what they were expected to respond by an estimation from the properties of the study lists. Although we modified the DRM paradigm by using paired words to make the task more difficult and ensure activation in all four PFC regions,

Discussion

The main goal of the present study was to identify the interrelation between brain activity in the right and left PFC during episodic memory retrieval. The data obtained by fMRI and the functional connectivity analysis revealed strong functional interconnections between the posterior PFC on each side and the contralateral posterior PFC but only weak functional interconnections between the anterior PFC and the contralateral anterior PFC. The results also indicated the absence of strong

Acknowledgments

This study was supported by JSPS (Japan Society for the Promotion of Science) Grants-in-Aids for Scientific Research. We are grateful to everyone who participated in our study.

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