Chapter 30 Forgetting and Retrieval BRICE A. KUHL AND ANTHONY D. WAGNER Retrieval of episodic memories — conscious memories of GROSS ANATOMY AND CONNECTIVITY past events — often provides critical information that can OF THE PREFRONTAL CORTEX shape current thought and behavior. Although successful remembering is generally thought of as far more desir- In this chapter, we primarily focus on the role of the PFC able than forgetting, it is likely that forgetting is also an in regulating episodic retrieval and forgetting. Thus, before important component of an adaptive memory system considering specific classes of forgetting and their relation (M. C. Anderson, 2003; Bjork, 1989; Schacter, 1999). To to the PFC, it is worth briefly describing the gross anatomy fully understand the functioning of episodic memory, it is of the frontal lobes — namely, subregions within the PFC important to consider both the situations and mechanisms that putatively support distinct functional mechanisms. that lead to successful remembering as well as those that The prefrontal cortex is generally divided into ventro- contribute to forgetting. Indeed, the phenomena of remem- lateral, dorsolateral, frontopolar, and medial subregions bering and forgetting are intimately related — that is, we (Figure 30.1). In the human, the ventrolateral PFC (VLPFC; often forget precisely because we have remembered some Figure 30.1A ) corresponds to the inferior frontal gyrus, other information. What we ultimately remember and for- which includes, from the caudal to rostral extent, inferior get is influenced both by our prior mnemonic experiences frontal pars opercularis (Brodmann Area [BA] 44), inferior as well as the functioning of neurobiological mechanisms frontal pars triangularis (BA 45), and inferior frontal pars that guide mnemonic retrieval. In particular, the frontal orbitalis (an area Petrides & Pandya, 2002, term area 47/12). lobes — which are known to play an important role in goal - Although Petrides and Pandya (2002) refer to area 47/12 directed attention and behavior —are central to the ability and BA 45 collectively as the mid - VLPFC, distinguishing to direct retrieval toward those memories that are relevant these regions from caudally situated BA 44, in this review, and away from those that are irrelevant. we highlight functional dissociations between area 47/12 We consider two broad classes of forgetting and their and area 45. Thus, we refer to inferior frontal pars orbit- corresponding relations to frontal lobe function. First, alis (area 47/12) as the anterior VLPFC, pars triangularis we review evidence that our ability to remember is often (BA 45) as the mid - VLPFC, and pars opercularis (BA 44) complicated by interference from competing memories, as the posterior VLPFC. The VLPFC is separated from the and that these situations (a) increase the likelihood of for- dorsolateral PFC (DLPFC) by the inferior frontal sulcus in getting and (b) increase demands on the prefrontal cortex humans (in monkeys, the principal sulcus marks this bound- (PFC). Second, we consider situations in which our mne- ary). Although DLPFC has been used to refer to a broad monic activities require selecting against, or avoiding, range of lateral PFC regions, we use DLPFC to refer to the particular memories, describing evidence that such acts middle frontal gyrus. As we discuss, episodic retrieval and of selection (a) increase the likelihood of later forgetting forgetting have been linked with activity in BA ’s 46 and 9/46 selected - against memories and (b) are supported by the (Figure 30.1A ) — subregions of DLPFC that Petrides and PFC. We conclude by situating the relationship between Pandya (1999) refer to as mid- DLPFC. Rostral to DLPFC the PFC and forgetting within the broader context of the and VLPFC is the frontopolar cortex (FPC; BA 10; Figure PFC and the control of cognition and behavior. 30.1A - B ). A final area of interest for the present chapter is the anterior cingulate cortex (ACC; BA ’ s 24 and 32; Figure 30.1B ), which is situated along the medial wall of the PFC, Supported by the National Institute of Mental Health (5R01 - immediately superior to the corpus callosum. MH080309 and 5R01 - MH076932) and the Alfred P. Sloan Importantly, PFC subregions are both interconnected Foundation. The authors thank Ben Levy for insightful discussion. and connected with posterior cortical sites, suggesting that 586 Handbook of Neuroscience for the Behavioral Science, edited by Gary G. Berntson and John T. Cacioppo. Copyright # 2009 John Wiley & Sons, Inc. cc30.indd30.indd 558686 88/18/09/18/09 66:27:43:27:43 PPMM Interference and Memory Retrieval 587 (A) retrosplenial cortex, DLPFC may interact with hippocam- pal and parahippocampal structures (Petrides, 2005). The 8B 4 FPC is connected both with the DLPFC and VLPFC as 8Ad 6 well as with the superior temporal cortex, cingulate cortex, 9 and retrosplenial cortex, suggesting that the FPC may be 9/46d 8Av particularly well suited to incorporate diverse sources of information (Petrides, 2005; Petrides & Pandya, 2007). The ACC is also widely connected with cortical sites, including 9/46v 6 multiple lateral PFC sites (DLPFC, in particular), the pos- 46 44 terior parietal cortex, and the medial temporal lobe cortex (Pandya, Van Hoesen, & Mesulam, 1981). Thus, whereas 45A 45B DLPFC and VLPFC have fairly distinct patterns of con- 10 nectivity with the posterior cortical sites, the FPC and ACC 47/12 may each interact with both DLPFC and VLPFC structures in coordinating goal - directed behavior. (B) 8B INTERFERENCE AND MEMORY RETRIEVAL 9 Perhaps the most widely accepted and well - documented cause of forgetting is interference. Interference occurs whenever irrelevant memories compete with relevant 24 CC memories (Mensink & Raaijmakers, 1988; for reviews, 32 see M. C. Anderson & Spellman, 1995; Wixted, 2004). The extent to which interference contributes to forgetting 10 is related both to the number of irrelevant memories that 25 compete as well as the strength of these irrelevant memo- ries. Most typically, interference is thought to occur dur- 14 ing the act of retrieval, creating situations of retrieval competition. Retrieval competition has been particularly well studied in three classic behavioral paradigms. First, Figure 30.1 A: Lateral view of the PFC and corresponding memories of past experiences often interfere with our abil- cytoarchitectonic areas. B: Medial view of the PFC. ity to retrieve memories of more recent experiences — a Note. (A) DLPFC ϭ Areas 46 and 9/46. VLPFC ϭ Areas 47/12, 45, and situation termed proactive interference. Conversely, the 44. FPC ϭ Area 10. (B) ACC ϭ Areas 32 and 24. From “ Dorsolateral ability to retrieve memories of past experiences is often Prefrontal Cortex: Comparative Cytoarchitectonic Analysis in the Human subject to interference from more recent memories — retro- and the Macaque Brain and Corticocortical Connection Patterns, ” by M. Petrides and D. N. Pandya, 1999, European Journal of Neuroscience, active interference. Finally, even when the order of learn- 11, pp. 1011 – 1036. Copyright 1999 by Blackwell Publishing. Reprinted ing is not relevant, the general principle that associates of with permission. a retrieval cue compete with each other during retrieval has been studied in the fan effect (J. R. Anderson, 1974). In the following sections, we briefly review first the clas- PFC subregions are well equipped to coordinate diverse sic behavioral evidence concerning these three situations cognitive operations. For example, the VLPFC is strongly of interference and then potential neurobiological mecha- connected with cortical areas in the lateral and medial tem- nisms that serve to overcome interference. poral lobe, including (but not limited to) the inferotempo- ral cortex, superior temporal cortex, and, more medially, Classic Interference Phenomena the perirhinal and parahippocampal cortex (Petrides & Pandya, 2002). The DLPFC has substantial reciprocal con- Proactive interference (PI) and retroactive interference nections with posterior parietal cortex, superior temporal cor- (RI) have been the subject of extensive behavioral research tex, retrosplenial cortex, anterior and posterior cingulate (for reviews, see M. C. Anderson & Spellman, 1995; cortex, as well as connectivity with VLPFC (Petrides & Wixted, 2004), and have been best illustrated in classic Pandya, 1999). Notably, through its connections with the A - B, A - C paradigms (Figure 30.2 ). In a standard A - B, A - C cc30.indd30.indd SSec1:587ec1:587 88/18/09/18/09 66:27:43:27:43 PPMM 588 Forgetting and Retrieval Retroactive Interference with the magnitude of RI decreasing as the delay increases A–B, A–C A–B, Filler (Postman, Stark, & Fraser, 1968). Target list Learn A–B Learn A–B Importantly, both of these properties of PI/RI can be well explained in terms of retrieval competition that occurs dur- Manipulation Learn A–C Filler Time ing cued recall (McGeoch, 1942; Mensink & Raaijmakers, Test for B: 1988). That is, an A - B, A - C paradigm elicits greater RI Ϫ A ? Worse Better than an A - B, C - D paradigm because the A - B, A - C para- Proactive Interference digm creates a situation in which a single retrieval cue (A) A–B, A–C Filler, A–C is linked to two associates — thereby enhancing retrieval Manipulation Learn A–B Filler competition and, therefore, the likelihood of forgetting. Similarly, changes in the relative magnitude of RI and PI at Target list Learn A–C Learn A–C Time different delays can be explained in terms of changes in the Test for C: relative salience of B and C terms and, therefore, changes AϪ ? Worse Better in retrieval competition. For example, some models sug- Figure 30.2 Schematic of retroactive interference and proac- gest differential decay rates for B and C terms following tive interference paradigms. A - C study, meaning that the relative strengths of the associ- Note. In both paradigms, the association between a cue (A term) and ate terms change with time (J. R. Anderson, 1983b). Other multiple associates (B & C terms) increases interference and, therefore, models suggest that changes in the availability of contex- forgetting.