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, Srinivas, & Weldon, in that participants reported more target items for stud- 1989). ied categories than for baseline categories. Most impor- In the present study, performance was assessed on tantly, there was a sigtllficant interaction of the two both implicit and explicit tests of conceptual memory. factors [F(1,17) = 15.43,MSe = 1.311,indicating that the The study was aimed at assessing whether there is a difference between studied and baseline item produc- semantic processing deficit in patients with frontal le- tion was reduced for the frontal patients. Specifically, sions. Both implicit and explicit conceptual tests benefit analysis of simple effects revealed that the performance from deep processing of word meanings, as indicated by of the two groups differed for studied items [F(l, 17) = their sensitivity to level of processing effects. Perfor- 18.93, MSe = 3.081 but not for baseline items [F(1, 17) mance on explicit tests is additionally benefited by the = 0.67, MSe = 2.421. Thus, frontal patients exhibited
I06 Journal of Cognitive Neuroscience Volume 9, Number I Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 1 2 3 4 5 6 7
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Figure 1. Computer-reconstructedlesions of patients with frontal lobe lesions due to stroke. For each patient, the lateral view on the far left shows the lesion projected onto the lateral surface of the brain. The horizontal cuts, from left to right, go from most inferior to most superior
impaired explicit categoryxued recall compared to their indicating that this priming effect was of comparable controls.' magnitude for patients and controls. If anything, the For the implicit test condition, the group (frontal vs priming effect was numerically greater for patients than control) by study condition (studied vs baseline) analysis for controls. revealed main effects of both factors. Frontal patients Despite the lack of interaction of group with priming, produced fewer target items overall than did controls the main effect of group suggested that the performance [F(1, 17) = 8.62,MSe = 4.581, and participants reported of the groups differed in some way. Analysis of simple more target items for studied categories than for baseline effects revealed that frontal patients produced fewer categories [F(1,17) = 36.06, MSe = 2.891.This difference baseline items than controls [F(1, 17) = 17.53, MSe = between production of studied items and chance pre 2.221. This finding of a difference in baseline perfor- duction of baseline items indicates that there was sig- mance between the two participant groups may be of nificant priming in the implicit category production test. concern. In particular, it could call into question the Furthermore, the interaction of the two factors did not interpretation of the finding of equal priming effects in reach significance [F(1,17) = 2.22,p = O.lG,MSe= 2.891, frontal patients and controls. For example, it could be
Gersbberg 107
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 pants), frontal patients may have had more difficulty 100 producing responses. Indeed, analysis of the number of responses produced by each participant revealed that frontal patients produced fewer responses than did con- 80 trols [F(1, 17) = 6.61,MSe = 13.221. Control participants - produced an average of 93.0 responses out of a possible (0 0 total of 96 (96.9%)for the testing session,whereas fron- 60 tal patients produced an average of 86.7 out of 96 c
C (90.3%)responses. Thus, the frontal patients may have 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 Q) produced fewer baseline items because they produced f 40 fewer items overall. n To assess whether the difference in baseline respond- 20 ing was indeed due to a difference in response produc- tion, additional analyses were conducted using only the first four responses produced for each category cue. Because participants were nearly always able to produce Control Frontal Control Frontal at least four responses for each cue, the groups did not Implicit Explicit differ in the number of responses produced [F( 1, 17) = 2.49,p = 0.13, MSe = 0.331. Control participants pro- duced an average of 47.8 responses out of a possible Figure 2. Experiment 1: Performance on implicit category produc- total of 48 (99.5%),and frontal patients produced an tion and explicit categorycued recall tests of memory for catego- rized lists as a function of participant group. Shaded portion of eacl- average of 47.4 out of 48 (98.8%)responses. So, if the column indicates baseline guessing rate. In aU figures, error bars indi- baseline difference in the implicit test condition was due cate standard error of the mean. to a difference in response production, there should be no baseline difference with the first four responses, for which response production was equal. Nonetheless, argued that frontal patients showed proportionately there was a trend toward a difference between the two greater priming than control participants. Therefore, an groups in production of baseline items in the first four explanation for the baseline difference was sought. One responses in the implicit test condition [F( 1,17) = 3.17, possibility is that the frontal patients produced fewer p = 0.09,MSe = 1.791. preselected baseline items because they produced fewer This trend toward a baseline difference even in the responses overall-participants were allowed to give first four responses suggests that the patients’ baseline fewer than eight responses for a category if they could deficit may not be attributable entirely to a reduction in not think of any more than they had given. Because of the number of responses produced. Subjective examina- their general difficulty in verbal fluency (see Partici- tion of the patients’ responses leaves the impression that
Table 1. Individual Memory Performance:Number of Target Items Produced (out of 15)
Experiment I Expmhaent 2 Implicit Explicit Implicit Explicit Patient Studied Baseline Studied Baseline Studied Baseline Studied Baseline
1. EB 5 2 10 6 4 1 6 6 2.MM 9 3 7 4 3 2 7 1 3. JD 6 2 5 2 2 1 1 1 4. KK 7 3 9 6 3 0 6 3 5. AL 12 3 11 6 7 1 10 2 6. RM 7 7 8 3 1 2 7 0 7. RT 7 3 8 2 4 2 4 1
MEANS Frontal 7.57 3.29 8.29 4.14 3.42 1.29 5.86 2.00 Control 8.83 6.25 11.92 4.75 5.00 2.50 8.50 1.67
108 Journal of Cognitive Neuroscience Volume 9, Number I Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 Figure 3 displays performance on the tests of free 100 recall that followed the implicit category production and explicit category-cued recall tests. As has been found in previous studies (Gershberg & Shimamura, 1995;Hirst & 80 Volpe, 1988; Incisa della Rocchetta, 1986; Incisa della - Rocchetta & Milner, 1993;Jetter et al., 1986;Stuss et al., 0 + 1994), the patients with frontal lesions exhibited im- 60 + K paired recall of the categorized lists. Analysis of variance,
c with group (frontal vs control) and type of prior test 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 c T (implicit vs explicit) as factors, confirmed the recall 40 deficit, revealing a main effect of group [F(1,17)= 32.13, a! MSe = 8.131.There was no main effect of prior test [F(1, 20 17) = 1.95,MSe = 3.761, but there was an interaction of the two factors [F(1,17) = 6.48,MSe = 3.761.Analysis of simple effects revealed that frontal patients recalled -- fewer words from the list tested with explicit cued recall First Second First Second than they had recalled from the list tested with implicit List List List List Control Frontal category production [F(l, 17) = 6.15, MSe = 3.761, but control participants did not show this effect [F(1, 17) = 0.90,MSe = 3.761. Figure 3. Experiment 1: Free recall of categorized lists as a func- This decrement in recall performance for the list that tion of participant pupand first vs second list studied in the had been tested explicitly compared to the list that had session. been tested implicitly may actually have been the result of the frontal patients exhibiting excessive sensitivity to proactive interference. That is, the list that was tested they may have had difficulty confining their responses with implicit category production was always studied to a particular category (e.g., “cut hand” for the category first in the session, and the list tested with explicit “diseases,” “snail” for the category “kinds of fish”) and category-cued recall was always studied second. So, hav- tended to give less common exemplars (e.g., “davenport” ing learned the first list may have interfered with learn- for the category “furniture,”“watercress” for the cate- ing the second list, at least for frontal patients. This effect gory “herbs and spices”).This issue of the quality of the was somewhat unexpected-in a prior study, such inter- patients’ responses-and its relation to the status of their ference effects in list learning were not found in frontal semantic memory, their ability to execute strategic patients when lists were made up of different categories search of semantic memory, and their deficits in verbal (Gershberg & Shimamura, 1995)-and the present study fluency-may be of interest for future research. was not intended to address interference effects. Indeed, To assess whether the difference in overall response the interference effect in free recall observed in the production may have affected the primary findings of present study could be problematic, because it parallels impaired cued recall and intact priming, production of the finding of impaired category-cued recall. That is, target items within the first four responses was analyzed. performance on both the implicit category production This analysis revealed the same patterns of effects as did test and the free recall test for the first list was less the analysis of total performance. Specifically,for explicit impaired than was performance on the explicit cued category-cued recall, analysis of variance revealed a recall test and the free recall test for the second list. group by study condition interaction [F(1, 17) = 38.98, Experiment 2 was conducted in an attempt to provide MSe = 0.941 in addition to main effects of group [F(1, additional evidence regarding the status of implicit and 17) = 17.38,MSe = 2.201 and study condition [F(1, 17) explicit conceptual memory in frontal patients. = 327.90, MSe = 0.941. The performance of the two groups differed for studied items [F(l, 17) = 36.1 1, MSe EXPERIMENT 2 = 2.071 but not for baseline items [F(1, 17) = 0.01,MSe = 1.061.For implicit category production, only the main Experiment 2 was conducted to provide a replication of effect of study condition-the priming effect-was sig- the major findings of Experiment 1, using a somewhat nificant [F(l, 17) = 32.82,MSe= 2.60l.There was neither different type of materials. For Experiment 2, the study an effect of group [F(l, 17) = 0.96,MSe = 2.531 nor an lists were organized on the basis of associative relation- interaction of the two factors [F(l, 17) = 1.25, MSe = ships rather than category membership. That is, each list 2.601. Thus, for the first four responses to each cue, was made up of clusters of words that were associatively frontal patients exhibited impaired explicit category- related to a common word. For example, the words cued recall but normal implicit category production “hunter,” “tamer,” “mane,” ‘king,” and “circus” are all priming. associative responses to the word ‘lion.”Because of the
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 nature of the study materials, the implicit test instruc- 2.061. The lack of interaction indicates that the priming tions were changed from category production to free effect was of comparable magnitude for patients and association-participants were given single words and controls. Furthermore, the patients’ performance did not told to say the first related words that came to mind (see differ from that of controls for either studied items [F(1, Shimamura & Squire, 1984). 17) = 2.59,p = 0.13,MSe = 4.581 or baseline items [F(1, 17) = 1.96,MSe = 3.321. Thus, frontal patients exhibited normal performance on the implicit free association test. Results and Discussion Figure 5 displays free recall performance for the asso- Figure 4 displays the performance of the group of pa- ciative lists. As in Experiment 1, analysis of variance 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 tients with frontal lesions and the control group on the revealed a main effect of group [F(l,17) = 24.95,MSe = tests of implicit free association and explicit associate- 8.161, with frontal patients recalling fewer words than cued recall. The performance of individual patients is control participants. Yet there was neither a main effect given in Table 1. The data from the two test conditions of preceding test type [F(1,17) = 0.24,MSe = 3.761 nor were analyzed in separate analyses of variance, each with an interaction [F(l,17) = 0.08,MSe = 3.761.Thus, despite two factors: participant group (frontal vs control) and the confounding of test type and study order, the finding study condition (studied vs baseline). For the explicit of impaired associatecued recall was not paralleled by test condition, the effect of group did not reach sig- an interference effect in free recall in the frontal nificance [F(l, 17) = 3.12, p = 0.10, MSe = 3.781, but patients. there was a significant effect of study condition [F(1,17) = 61.13,MSe = 4.131 and a significant interaction of the GENERAL DISCUSSION two factors [F(l, 17) = 4.74, MSe = 4.131. Analysis of simple effects revealed that the performance of the two In two experiments, the performance of patients with groups differed for studied items [F(1,17) = 5.72,MSe = frontal lobe lesions was examined on implicit and ex- 5.401 but not for baseline items [F(1, 17) = 0.20,MSe = plicit tests of conceptual memory for organized lists of 2.511. Thus, frontal patients exhibited impaired explicit words. Frontal patients exhibited normal levels of con- associatecued recall.* ceptual priming on implicit tests, but they exhibited For the implicit test condition, the group by study impaired cued recall on explicit tests. Both implicit and condition analysis revealed only a main effect of study explicit conceptual tests are sensitive to level of process- condition. Thus, there was a significant priming effect ing effects (Hamann, 1990; Roediger et al., 1989). Thus, [F(1, 17) = 23.19, MSe = 2.061 but neither an effect of these findings suggest that frontal patients do not have group [F(1, 17) = 3.13,p = 0.09, MSe = 5.481 nor an a basic deficit in semantic processing of individual items. interaction of the two factors [F(1, 17) = 0.14, MSe = Rather, their cued recall deficit may be related to their
100 100
80 80 - - 0 e 8 60 8 60 U U c rh CI C C 40 40 nP) z T T 20 20 1
Control Frontal Control Frontal
Implicit Explicit List ~ List List List Control Frontal
Figure 4. Experiment 2: Performance on implicit free association and explicit associatecued recall tests of memory for associatively Figure 5. Experiment 2: Free recall of associatively organized lists organized lists as a function of participant group. Shaded portion as a function of participant group and first vs second list studied in of each column indicates baseline guessing rate. the session.
110 Journal of Cognitive Neuroscience Volume 9,Number 1
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 deficits in the use of organizational encoding and strate- findings of frontal lobe activation during the perfor- gic retrieval processes (Gershberg & Shimamura, 1995). mance of semantic processing tasks (Dkmonet et al., The finding that frontal patients exhibited impaired 1992; Kapur et al., 1994a, 1994b; Petersen et al., 1988, performance on explicit tests of cued recall suggests that 1989; Posner et al., 1988; Tulving et al., 1994)? One the memory deficits of these patients may not be limited possibility is that prefrontal cortex is normally recruited to retrieval processes. Some past studies have suggested but is not necessary for semantic processing. Yet, even that frontal patients exhibit only retrieval deficits (Incisa within the functional imaging literature, several studies della Rocchetta & Milner, 1993; Jetter et al., 1986), have reported conflicting findings and alternative inter-
whereas another has provided evidence for both encod- pretations of the activation of prefrontal cortex during 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 ing and retrieval deficits (Gershberg & Shimamura, semantic processing tasks (Grasby, Frith, Friston, Bench, 1995). In the present study, although normal implicit test Frackowiak, & Dolan, 1993; Kapur et al., 1994b; Shallice, performance suggests normal semantic processing of Fletcher, Frith, Grasby, Frackowiak, & Dolan, 1994; Tulv- individual items in patients with frontal lobe lesions, ing et al., 1994). In these studies, prefrontal cortex acti- impaired explicit test performance suggests that other vation was specifically associated with tasks that encoding processes may be impaired. That is, because required or promoted storage of words in long-term the explicit tests provided organizing cues (e.g., category memory. These findings were interpreted as indicating names), the need for strategic retrieval processes was that dorsolateral prefrontal cortex may play a particular reduced. Thus, the impaired performance exhibited by role in episodic or elaborative encoding processes rather the patients on the explicit tests may reflect poor organ- than a more general role in semantic analysis (Grasby et izational processing at encoding as well as impaired al., 1993;Kapur et al., 1994b;Shallice et al., 1994;Tulving strategic retrieval. et al., 1994). Thus, frontal lobe activation revealed in These results may also be relevant to the issue of functional imaging studies of semantic processing may whether implicit conceptual tests are sensitive to vari- reflect the same sort of strategic, organizational encod- ations in organizational processing. The present study ing processes as are impaired in patients with frontal examined patients who, on tests of free recall in a past lobe lesions (e.g., Gershberg & Shimamura, 1995). Such study, exhibited deficits in use of organizational strate- processes may have been executed by normal individu- gies, including category clustering (Gershberg & Shima- als even when they were not explicitly required to do mum, 1995). Under the present intentional learning so by the tasks used in the imaging studies. conditions, controls presumably engaged in more organ- In summary, patients with frontal lobe lesions exhib- izational processing than did frontal patients. Nonethe- ited normal Performance on implicit conceptual tests less, the patients performed normally on implicit but impaired performance on parallel explicit tests of conceptual tests of memory for organized lists. Further- memory for organized lists of words. These findings more, a similar study of implicit and explicit memory appear to rule out a deficit in semantic processing of performance in schizophrenic patients, who have also individual list items as an explanation of the memory been found to exhibit deficits in use of organizational impairments associated with frontal lobe damage. Rather, strategies such as category clustering (Koh, Kayton, & impaired cued recall performance suggests that strategic, Berry, 1973), revealed a similar pattern of results as the organizational memory processes are impaired in pa- present study. Specifically, schizophrenic patients exhib- tients with frontal lobe lesions. Incidental engagement ited normal implicit category production priming but of such organizational processes may be the source of impaired explicit category-cued recall (Schwartz, Rosse, activation in prefrontal cortex revealed during semantic & Deutsch, 1993). In contrast, a past study (Rappold & processing tasks in functional imaging studies. Together, Hashtroudi, 1991) suggested that category production this interpretation of past imaging studies and the results priming was affected by varying organizational process- of the present neuropsychological study are consistent ing, based on the finding that priming increased when with the view that the deficits in memory and strategy participants were instructed to use a categorization strat- use exhibited by patients with frontal lobe lesions are egy or were given blocked presentation of a categorized related to a more general deficit in executive control of list. Yet, the findings for patient populations suggest that working memory. implicit conceptual tests such as category production may not be affected by organization. In the Rappold and Hashtroudi (1991) study, strategy instruction and list METHODS organization may have affected performance because of Experiment 1 use of explicit retrieval by the college student partici- pants. Alternatively, these implicit tests may have only Participants limited sensitivity to organizational factors, with perfor- Patients with frontal lobe lesions. Seven patients with mance varying only when organization is made particu- unilateral frontal lobe lesions (five left and two right) larly salient. were tested. The patients were identified by review of How can the present findings be reconciled with medical records and computed tomography (cT> or
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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 magnetic resonance (MR) scans at the Veterans Affairs The patients (five men and two women) averaged Outpatient Clinic in Martinez, CA. Potential participants 67.9 years of age and 14.0 years of education (Table 2). were included if medical records indicated a history of They scored within normal range on standard tests of a single cerebral vascular accident at least one year prior intelligence and memory (Table 3). On the Wechsler to testing (range: 7- 13 years) and no history of any other Adult Intelligence Scale-Revised (WAIS-R), they had an sigtlLficant medical, neurological, or psychiatric disorder average full scale score of 97.0.Their mean scores on the (e.g., substance abuse, head injury, dementia, depression). five scales of the Wechsler Memory Scale-Revised For each of the patients included in the study, the lesion (WMS-R) were: Attention = 87.7,General = 94.6,Delayed
was in the territory of the precentral branch of the Memory = 100.6, Verbal Memory = 87.6, and Visual 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 middle cerebral artery and included dorsolateral prefron- Memory = 90.9. The patients exhibited impairment on tal cortex (Fig. 1). Based on quantitative analysis of the two neuropsychological tests that are sensitive to frontal neuroimaging data, the average lesion volume was esti- lobe damage. On the Wisconsin Card Sorting Test (Hea- mated at 31.1 cm3 (range: 10.3-52.1 cm3). ton, 1981), they achieved fewer categories [K17) = 2.06,
Table 2. Participant Characteristics
Lesion Education Patient side volume (cm3) (years) Age at test Sex 1. EB right 17.3 12 75 F 2.MM right 52.1 12 67 M
3. JD left 30.8 20 65 M 4. KK left 17.4 13 61 M 5.AL left 51.2 13 63 F 6. RM left 10.3 12 67 M 7. RT left 38.7 16 77 M
MEANS Frontal 2R,5L 31.1 14.0 67.9 5M,2F Control - - 14.8 63.8 8 M,4 F
Table 3. Standardized Test Scores
WCST' WAS-R WMS-R Patient FSIQ~ Generalb Cat. RE. FAY BNT~ 1. EB 107 91 4 32 48 53 2.MM 94 93 0 92 12 50 3. JD 93 87 6 15 8 43 4. KK 107 100 4 51 31 56 5. AL 104 109 4 11 21 50 6. RM 88 90 6 15 24 46 7. RT 86 92 2 22 9 43
MEANS Frontal 97.0 94.6 3.7 34.0 21.9 48.7 Control - - 5.3 12.0 43.0 57.3
a Wechsler Adult Intelligence Scale-Revised, Full Scale IQ. Wechsler Memory Scale-Revised, General Memory Index. Wisconsin Card Sorting Test (Heaton, 1981)-number of categories achieved (Cat.) and number of perseverative errors (PIE.). FAS Verbal Fluency Test (Benton & Hamsher, 1978)-total number of words produced in three minutes. Boston Naming Test (Kaplan, Goodglass, & Weintraub, 1983)-number correct out of 60.
I I2 Journal of Cognitive Neuroscience Volume 9, Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 p = 0.051 and made more perseverative errors than was randomized for each participant, with the restriction control participants [t(17) = 2.421, and on the FAS Verbal that no two items from the same category were pre- Fluency Test (Benton & Hamsher, 1978), the patients sented adjacently. At test, category cues were presented produced fewer words in three minutes than control sequentially, each for an unlimited time. Presentation participants [t(17) = 3.231. order was randomized for each participant, with target The patients were screened for language disorders. categories and baseline categories intermixed. The criterion for inclusion in the study was a score of at least 85 on the Western Aphasia Battery (Kertesz, 1982). This criterion served to exclude individuals with Procedure 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 moderate to severe aphasia. However, as is common in patients with frontal lobe lesions, some of the patients Each participant was tested individually in a single ses had mild dysfluency or difficulty in word-finding. Spe- sion. Participants were shown fifteen words, one at a cifically, on the Boston Naming Test (Kaplan, Goodglass, time, and they were instructed to read each word aloud & Weintraub, 1983), the patients spontaneously named and to try to remember the words. After all fifteen words fewer pictures than control participants [t(17) = 4.551. in the list were presented, the words were presented for study a second time in a different, random order. Control participants. Twelve healthy volunteers (eight Following presentation of the word list, participants men and four women) at the Martinez VA Clinic served were told that some other tasks would be administered as controls for the patients. They were matched with the before their memory was tested. A filler task was given patients with frontal lobe lesions on the basis of age to provide a delay between study and test and to estab- [t(17) = 1.281 and education [t(17) = 0.57].However,the lish an implicit mode of responding. Nine letters of the control participants performed better than the frontal alphabet were presented one at a time, at a rate of ten patients on several subtests of the WAIS-R: Vocabulary, seconds per letter. Participants were asked to say a per- t(17) = 3.64; Information, t(17) = 2.55; and Digit-Symbol, son’s first name beginning with each letter. Half of the t(17) = 3.10. participants were asked to give female names, and the other half were asked to give male names. The name responses were recorded by the experimenter. Materials and Apparatus Immediately following the 90-second filler task, par- The materials for Experiment 1 were drawn from the ticipants were given the implicit category production Battig and Montague (1969) category norms. From each test. They were not told that this was a memory test. of twelve categories (e.g., furniture, weapons, trees), five Participants were shown category cues and instructed common exemplars were selected (e.g., desk, bed, to say the first eight members of each category that couch, cabinet, lamp). In terms of overall production came to mind. Prior to testing, a practice trial was given. frequency, the selected exemplars had an average rank- The experimenter gave the practice cue (e.g., sports) ing of 8.5 (range: 3-22); the two topranked items from and two exemplars (football, hockey) and asked the each category were excluded. The exemplars had a participant to provide additional exemplars that fit the mean word frequency of 52 per million (Francis & category. Participants were told that some of the catego- Kucera, 1982). From these materials, four lists of fifteen ries might relate to words they had studied but that they words were constructed, each consisting of five exem- should not be concerned with this issue. It was empha- plars from each of three categories. The four lists were sized that they should say the very first words to come divided into two pairs, such that the two lists in each to mind, without considering whether or not they had pair were matched for word frequency. For each partici- been studied. Previous findings suggest that these in- pant, one pair of lists was used for the implicit test of structions facilitate implicit retrieval (Schacter, Bowers, memory and the other pair was used for the explicit test. & Booker, 1989). Within each test, one list served as the studied target list, The six category names-three corresponding to stud- and the other list served as the unstudied baseline list. ied words and three corresponding to unstudied base- The names of the categories used in the studied and line items-were presented in a random order for each baseline lists served as test cues. Assignment of lists to participant, with target categories and baseline catego- implicit and explicit test conditions and to target and ries intermixed. Responses were recorded by the experi- baseline study conditions was counterbalanced across menter. Participants were given as much time as they participants. needed to produce the eight responses for each cate- Study lists and test cues were presented on a Macin- gory (controls: average = 50.0 seconds per category; tosh computer, in the center of the screen, in a %-point, frontal patients: average = 109.2 seconds per category). unserifed font. Study words were printed in lowercase Some participants were not able to produce eight re- letters, and test cues were printed in uppercase letters. sponses for every category. Participants were encour- At study, the fifteen words were presented sequentially, aged to give as many responses as they could, but when at a rate of five seconds per word. Presentation order a participant indicated that he or she was not able to
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Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 think of any new responses for a category, the experi- constructed, each consisting of five associates of each of menter went on to the next category. three cue words. The four lists were divided into two After the implicit category production test, partici- pairs, which were matched for associate ranking and pants were given a test of free recall for the studied word frequency. For each participant, one pair of lists words. This test fulfilled the participants’ expectations of was used for the implicit test of memory, and the other a memory test. They were asked to report as many of the was used for the explicit test. For each test, one of the studied words as they could remember, and their re- lists in the pair served as the studied target list, and the sponses were recorded by the experimenter. There was other list served as the unstudied baseline list. Assign-
no time limit for free recall, which generally took about ment of lists to implicit and explicit test conditions and 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 one minute. For the next ten minutes, to provide a break to target and baseline study conditions was counterbal- from verbal memory tasks, the participants participated anced across participants. in a nonverbal reaction time task that was part of an- other study. Following the break, the above procedures were re- Procedure peated for the explicit category-cued recall test. The procedures were identical, except for the instructions The procedures used in Experiment 2 were identical to given prior to the presentation of the category names. those used in Experiment 1, with one major exception: That is, participants were given two study presentations the instructions given for the implicit and explicit tests of a list of fifteen words. The name generation filler task of memory were different from those used in Experi- was conducted using nine letters of the alphabet differ- ment 1 because of the different nature of the studied ent from those used during the implicit task. For the materials. That is, for the implicit test, a free association categorycued recall test, participants were instructed to test was given. Participants were told that they would be use the category cues to help them recall words from shown single words and that they should say the first the studied list. Participants were asked to try to recall eight words to come to mind that related to each cue as many studied words as they could that fit into each word (average time to respond: control = 48.0 seconds category. In fact, participants were asked to provide eight per cue; frontal = 109.8 seconds per cue). For the ex- responses for each category, even though there were not plicit test, an associatecued recall test was given. Partici- that many studied items for each category. Participants pants were told to use the cue words to help them recall were alerted to the fact that some of the categories words from the list that were related to the cue words would not correspond to any studied items, and they (average time to respond: control = 50.4 seconds per were told to simply provide any eight responses for such cue; frontal = 130.5 seconds per cue). In contrast to categories. (Average time to respond: control = 58.6 Experiment 1,all participants were required to give eight seconds per category, frontal = 135.4 seconds per cate- responses for every cue for both tests, and all partici- gory.) Finally, following the cued recall test, participants pants were able to meet this requirement. The name-gen- were asked for free recall of the studied list. eration filler task was again used between study and test, but the participants who had given male names in Ex- Experiment 2 periment 1 were asked to give female names in Experi- ment 2, and those who had given female names were Participants asked to give male names. The same seven patients with frontal lobe lesions and twelve control participants were tested in Experiment 2 as were tested in Experiment 1. For each participant, an Acknowledgments interval of at least three weeks was provided between testing in Experiment 1 and testing in Experiment 2. This research was supported by an NSF Graduate Research Fellowship to Felicia B. Gershberg and NIH Grants AGO9055 and MH48757 to Arthur I? Shimamura. The experiments were Materials conducted as part of the requirements for the Ph.D. earned by Felicia B. Gershberg at the University of California at Berkeley. The materials for Experiment 2 were drawn from word Thanks to Arthur I? Shimamura for much valuable advice and association norms aenkins, 1970). For each of twelve guidance, Mieke Verfaellie for helpful comments on an earlier draft, Dr. Robert T. Knight and Dr. Robert Rafal for conducting cue words (e.g., baby, moon, lion), five common associa- neurological exams, screening patients, and providing testing tive responses were selected (e.g., diaper, bottle, crib, space, Jennifer A. Mangels and Paul J. Jurica for assistance in doll, rattle). In terms of overall production frequency, the neuropsychological testing, and Clay Clayworth for producing selected associates had an average ranking of 10.1 Figure 1. (range: 5-20); the four topranked responses to each Reprint requests should be sent to Felicia B. Gershberg, Mem- word were excluded. The associates had a mean word ory Disorders Research Center (1 5 1-A), Department of Veterans frequency of 51 per million (Francis & Kucera, 1982). Affairs Medical Center, 150 South Huntington Avenue, Boston, From these materials, four lists of fifteen words were MA 02130. E-mail:[email protected].
I14 Journal of Cognitive Neuroscience Volume 3,Number I Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.1.105 by guest on 01 October 2021 Notes Francis, W. N., & Kucera, H. (1982). Fwquency analysis of English usage: Lexicon and grammar Boston: Houghton 1. Some researchers have suggested that the memory func- Mifflin. tions of the left and right frontal lobes differ (e.g.,Tblving et Fuster, J. M. (1990). Prefrontal cortex and the bridging of tem- al., 1994). Therefore, an additional analysis was conducted in poral gaps in the perception-action cycle. In A. Diamond which the explicit category
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