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Beyond HERA: Contributions of Specific Prefrontal Brain Areas to Long-Term Memory Retrieval

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Beyond HERA: Contributions of Specific Prefrontal Brain Areas to Long-Term Memory Retrieval Psychonomic Bulletin & Review 1996,3 (2),149-158 Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval RANDY L, BUCKNER Washington University, si: Louis, Missouri Recent neuroimaging studies have provided a wealth of information about areas within prefrontal cortex involved in long-term memory, These studies prompted a proposal by Tulving and colleagues (Tulving, Kapur, Craik, Habib, & Houle, 1994)that prefrontal contributions to memory function are related to laterality differences (the hemispheric encoding/retrieval asymmetry model). This review goes beyond a general characterization of prefrontal lobes to a more specific analysis of distinct areas within the prefrontal cortex. Separate prefrontal areas, sometimes within the same hemi­ sphere, are discussed in terms of selective contributions that they might make to memory retrieval, In the end, it is concluded that a framework which tries to understand prefrontal function in terms of specific areas is a useful complement to models, like HERA,which attempt to find unifying prin­ ciples across multiple areas. The past decade has seen an outpouring of informa­ multiple neuroimaging studies conducted across several tion about the neurobiological basis ofhuman cognition, different laboratories. The main assertions of the HERA owing largely to the refinement ofmethods for imaging model were that (1) right prefrontal cortical areas are more active brain areas in healthy, awake subjects as they per­ involved in episodic retrieval than are left prefrontal areas, form cognitive tasks (Posner & Raichle, 1994). These and (2) left prefrontal areas are more involved in semantic methods, often referred to as neuroimaging techniques, retrieval and episodic encoding than are right prefrontal provide a window, previously unavailable, into the func­ areas. The idea that the prefrontal cortex may be involved tion ofthe brain. Memory research has likewise benefit­ in long-term memory function had been previously advo­ ted tremendously from these technologies, with over 50 cated on the basis oflesion work (Milner, Petrides, & Smith, imaging studies ofmemory reported to date. Importantly, 1985; Moscovitch, 1982; Schacter, 1987; Shimamura, these studies have allowed researchers to propose and Janowsky, & Squire, 1991), but hemispheric asymmetry in test ideas about brain areas and pathways that might un­ relation to memory function was a completely novel pro­ derlie memory function (for examples see Buckner & Tul­ posal which helped draw attention to the commonalities ving, 1995; Petrides, Alivisatos, Evans, & Meyer, 1993; observed across a wide range ofneuroimaging studies. Raichle et al., 1994; Schacter, Alpert, Savage, Rauch, & Recently, the HERA model has been revisited in order Albert, 1996). Many ofthe results are in good agreement to determine how well it has predicted new data (Nyberg, with predictions based on earlier methodologies; other Cabeza, & Tulving, 1996). The current scorecard, which results have been entirely unanticipated. includes data collected after HERA's initial report (Tul­ On the basis ofunexpected findings about the lateral­ ving, Kapur, Craik, et aI., 1994), is well in favor of HERA, ization of prefrontal activations during memory tasks, suggesting that the model reliably captures a general pat­ Tulving, Kapur, Craik, Moscovitch, and Houle (1994) pro­ tern observed across many neuroimaging studies. posed a model ofhemispheric encoding/retrieval asym­ However, in spite ofthe HERA model's ability to pre­ metry (HERA). The HERA model drew on data from dict data on the average, several ofits shortcomings need to be addressed. The HERA model's main limitation is that it is minimally constrained in terms of prefrontal I thank Steve Petersen, Julie Fiez, Adina Roskies, and Susan Court­ anatomy and thus provides only an initial heuristic from ney for helpful comments on various versions ofthis manuscript and which to work. A second limitation is that the model fo­ Dan Schacter, Roger Ratcliff, John Gabrieli, Henry Roediger, and an cuses on prefrontal brain areas that differ across stages anonymous reviewer for thoughtful comments during the review process. Support was provided by NIH Grant NS32979 and grants and types of memory, while it underemphasizes com­ from the Charles A. Dana Foundation and the McDonnell Center for monalities-which may also be quite important. Higher Brain Function. The present research was conducted at Wash­ In this review, attention will be focused on a finer level ington University School ofMedicine, Department ofNeurology and of prefrontal analysis in line with our current under­ Neurological Surgery. Correspondence concerning this article should be sent to R. L. Buckner, MGH-NMR Center, 13th St., Building 149, standing ofprefrontal anatomy. This should not be taken Room 2301, Charlestown, MA 02129 (e-mail: [email protected]. as a step backward. The goal is not to show that the HERA harvard.edu). model is inaccurate, but rather to provide a more detailed 149 Copyright 1996 Psychonomic Society, Inc. 150 BUCKNER look at which prefrontal areas are involved in memory with regard to the human prefrontal cortex, it is essential function, and in what capacities. This is meant as a step to begin a functional characterization with the assump­ forward and as a complement to the HERA model. tion that multiple areas exist which may perform separa­ Evidence shows that neuroimaging techniques are ca­ ble operations (Buckner & Petersen, 1996). pable of resolving distinct subdivisions (areas) of the Given this orientation, the natural question becomes, prefrontal cortex. Examination of the prefrontal cortex Are we technically capable ofstudying the multiple func­ in terms of specific areas should yield a more complete tional subdivisions of human prefrontal cortex? Using description ofprefrontal contributions to memory. Sev­ traditional methodologies, such as lesion analysis, it is eral examples will be given which show how multiple, often difficult to divide the prefrontal cortex into func­ functionally distinct prefrontal areas contribute to long­ tional areas because of the limited availability of focal term memory retrieval processes; some ofthese areas are brain injuries. However, such characterization is begin­ located in the right prefrontal cortex, while others are lo­ ning and is likely to make important contributions (e.g., cated in the left. Neuroimaging studies have revealed Fiez, Damasio, & Tranel; 1995; Swick & Knight, in press). distinct prefrontal areas which have selective roles in Neuroimaging methods, however, serve as a ready memory retrieval that are not captured by descriptions tool for characterizing distinct prefrontal areas. These based solely on their laterality. methods permit the observation oflocal changes in me­ tabolism that are correlated with focused changes in CONCEPTUAL CONSIDERATIONS neural activity (DeYoe, Bandettini, Neitz, Miller, & Multiple Prefrontal Areas and the Ability of Winans, 1994; Raichle, 1987). Moreover, there are data Neuroimaging to Detect Them that can be used to determine the current ability of neu­ roimaging to localize and resolve activations within the Before a description of prefrontal contributions to prefrontal cortex-locali::ation referring to the accuracy memory can be made, it is important to discuss what, ex­ with which an activation can be placed within the pre­ actly, the prefrontal cortex is. The prefrontal cortex is a frontal cortex, and resolution referring to the distance by subdivision of the frontal cortex, the most anterior por­ which two areas of activation must be separated before tion of the human brain. Unlike the primary motor cor­ they can be identified as more than one area. Localiza­ tex and premotor cortex, which are also subdivisions of tion and resolution are similar in that they both enable the frontal cortex, the prefrontal cortex does not have the accurate description ofan activation. However, mul­ connections to brain areas that directly control move­ tiple areas of activation can be indistinguishable (poor ment and thus must act indirectly (through the premotor resolution) but nonetheless consistently localized to the and motor cortex) to participate in the production of same large area (reliable localization). Similarly, multi­ overt behaviors. Anatomically, the prefrontal cortex is ple activated areas can consistently appear as separate defined by the organization ofits cortical layers at a mi­ activations (good resolution), but their locations can croscopic level, its connections to other brain areas such vary from one subject group to the next (unreliable lo­ as the thalamus, and physiological properties (Goldman­ calization). It is thus important to address localization Rakic, 1987). and resolution separately. It has long been accepted that the prefrontal cortex is The ability of neuroimaging to reliably localize pre­ made up of multiple, functionally distinct areas. Brod­ frontal brain areas is demonstrated in studies ofthe same mann (1909/1994), using purely anatomical techniques, behavioral paradigm across independent groups of sub­ characterized the human prefrontal cortex and described jects imaged on separate occasions. Figure IA shows such (with some uncertainty) eight distinct prefrontal areas. an example, in which a left prefrontal activation was de­ The map that he produced, which included these areas and tected across three independent groups of subjects per­ a few more added later, is now widely used as a common forming
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