Implicit and Explicit Conceptual Memory Following Frontal Lobe Damage Felicia B. Gershberg Boston University School of Medicine and Department of Veterans Affairs Medical Center Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/9/1/105/1755413/jocn.1997.9.1.105.pdf by guest on 18 May 2021 Abstract In two experiments, the performance of patients with fron- and associatecued recall tests. The findings of normal perfor- tal lobe lesions was examined on implicit and explicit tests of mance on implicit conceptual tests suggest that frontal patients conceptual memory for organized lists of words. Frontal pa- do not have a basic deficit in semantic processing of individual tients exhibited normal levels of conceptual priming on im- items. Impaired performance on explicit cued recall tests may plicit category production and free association tests, but they be related to deficits in the use of organizational encoding and exhibited impaired memory performance on explicit category- strategic retrieval processes. H INTRODUCTION prefrontal cortex in controlling working memory (e.g., Baddeley, 1986; Fuster, 1990; Goldman-Rakic, 1987; Damage to the frontal lobes results in memory impair- Moscovitch, 1993; Shimamura, 1994). In addition, func- ment across a variety of tasks, including tests of immedi- tional imaging studies have revealed activation of pre- ate memory span, memory for temporal and source frontal cortex during tasks that require executive control information, and metamemory aanowsky, Shimamura, of working memory (e.g., D’Esposito, Detre, Alsop, Lis- Kritchevsky, & Squire, 1989a; Janowsky, Shimamura, & terud, Atlas, & Grossman, 1994;Petrides, Alivisatos, Evans, Squire, 1989b; McAndrews & Milner, 1991; Milner, & Meyer, 1993;Petrides, Alivisatos, Meyer, & Evans, 1993). Petrides, & Smith, 1985; Shimamura,Janowsky, & Squire, An alternative to the working memory view is that the 1991). The memory deficits of patients with frontal lobe memory impairments of patients with frontal lobe le- lesions are particuIarly prominent on tests of free recall sions can be explained by a deficit in semantic process- (Eslinger & Grattan, 1994;Gershberg & Shimamura,1995; ing. By this view, impaired semantic processing could Hirst & Volpe, 1988; Incisa della Rocchetta, 1986; Incisa cause memory impairments in frontal patients because della Rocchetta & Milner, 1993;Janowsky et al., 1989a; of the role of level of processing in normal memory. That Jetter, Poser, Freeman, & Markowitsch, 1986; Stuss, Alex- is, because semantic processing at study results in better ander, Palumbo, Buckle, Sayer, & Pogue, 1994). Free recall memory performance than does lower-level (phonologi- performance depends heavily on the use of memory cal or graphemic) processing at study (Craik & Tulving, strategies, and patients with frontal lobe lesions exhibit 1975), impaired semantic processing would result in reduced use of organizational strategies such as category impaired memory. The possibility that the frontal lobes clustering and subjective organization @linger & Grat- play a role in semantic processing has been suggested tan, 1994; Gershberg & Shimamura, 1995; Stuss et al., by functional imaging studies. These studies have re- 1994). vealed heightened activation of lateral frontal cortex The present study was aimed at contrasting two pos- during the execution of tasks that require semantic proc- sible explanations of the recall and strategy use impair- essing of words, such as generating associated verbs or ments exhibited by patients with frontal lobe lesions. By determining their semantic categories, compared to sim- one view, these impairments can be explained by a ply reading or superficially processing words (Demonet, general deficit in executive control of working memory. Chollet, Ramsay, Cardebat, Nespoulous, Wise, Rascol, & That is, the recall impairments of frontal patients may Frackowiak, 1992;Kapur, Craik, Tulving, Wilson, Houle, & reflect the heavy working memory load required for the Brown, 1994a; Kapur, Rose, Liddle, Zapursky, Brown, selection and execution of effective memory strategies Stuss, Houle, & Tulving, 1994b; Petersen, Fox, Posner, (Gershberg & Shimamura,1995).Various theories of fron- Mintun, & Raichle, 1988, 1989; Posner, Petersen, Fox, & tal lobe function,based on work with nonhuman animals Raichle, 1988;Tulving, Kapur, Craik, Moscovitch, & Houle, as well as human patients, have suggested a role of 1994). 0 1997 Massachusetts Zmtitute of Technology Journal of Cognitive Neuroscience 9:1,pp. 105-116 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 In the present study, implicit and explicit tests of use of memory strategies at encoding and retrieval. Thus, conceptual memory were used to assess the semantic if frontal patients have a deficit in the use of explicit processing deficit hypothesis. In explicit tests of mem- memory strategies but not in semantic processing of ory, such as traditional tests of free recall, cued recall, individual items, then they should exhibit impairment and recognition memory, participants are instructed to only in explicit tests. Alternatively,if frontal patients have try to recollect a prior episode. In contrast, implicit tests a basic deficit in semantic processing, then they should of memory make no reference to any prior episode, and exhibit impairments in both implicit and explicit con- memory is inferred from changes from baseline perfor- ceptual tests. mance. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/9/1/105/1755413/jocn.1997.9.1.105.pdf by guest on 18 May 2021 Neuropsychological studies using implicit tests of memory have revealed that patients with amnesia ex- EXPERIMENT 1 hibit normal performance on most implicit tests despite severely impaired performance on most explicit tests of In Experiment 1, patients with frontal lobe lesions memory (for review, see Schacter, 1987; Shimamura, (Fig. 1) and age- and education-matched control partici- 1986,1993).Thus, performance on implicit tests of mem- pants were given tests of implicit category production ory may be viewed as reflecting the facilitatory effects and explicit category-cued recall. For both tasks, partici- of prior processing on subsequent processing of the pants studied a randomly-arranged list of categorized same or related material, without the involvement of words. At test, participants were given category names conscious or strategic memory processes. Patients with as test cues. Half of the categories corresponded to frontal lobe lesions have been shown to perform nor- studied items, and half corresponded to baseline items mally on an implicit word-stem completion test (Shima- (items in a list studied by other subjects). The only difference between the tasks was the instructions mura, Gershberg, Jurica, Mangels, & Knight, 1992). The two given at test. For the implicit test, participants were performance of patients with frontal lobe lesions on other implicit tests of memory has not been reported instructed to report the first exemplars that came to prior to the present study. mind for each category cue. For the explicit test, partici- Cognitive studies of implicit memory have revealed pants were instructed to use the category cues as re- that some implicit tests primarily reflect the effects of trieval aids for the studied words. For both tests, prior lexical and perceptual processing, whereas other participants were asked to give eight responses for each implicit tests reflect the effects of prior conceptual proc- cue. Immediately after each of these tests, participants essing. That is, some implicit tests, such as word-stem were given a test of free recall for the same words. completion, provide cues that orient participants toward lexical and perceptual information. These tests are af- Results and Discussion fected by manipulations of surface features of stimuli (such as changes in presentation modality or typography Figure 2 displays the performance of the group of pa- between study and test) but not by manipulations of tients with frontal lesions and the control group on the level of processing at study (Jacoby, 1983; Jacoby & tests of implicit category production and explicit cate- Dallas, 1981; Roediger & Blaxton, 1987). Other implicit gory-cued recall. The performance of individual patients tests use cues that are semantically or associatively re- is given in Table 1.The data from the two test conditions lated to studied words. In such tests, participants may be were analyzed in separate analyses of variance, each with asked to produce members of categories following study two factors: participant group (frontal vs control) and of some exemplars of those categories or to “free asso- study condition (studied vs baseline). For all effects re- ciate” to cue words that are semantically related to stud- ported as si@cant,p < 0.05, unless noted otherwise. ied words (Graf, Shimamura, & Squire, 1985; Shimamura For the explicit test condition, this analysis revealed a & Squire, 1984). These implicit conceptual tests behave significant effect of group [F(l, 17) = 9.48, MSe = 4.191, like explicit tests in that they are affected by conceptual with frontal patients producing fewer target items over- manipulations such as level of processing but not by all than control subjects. There was also a significant manipulations of surface features (Hamann, 1990;Jacoby, effect of study condition [F(1,17) = 215.91,MSe= 1.311, 1983;Jacoby & Dallas, 1981; Roediger,