Frontal Verbal Amnesia Phonological Amnesia H. Branch Coslett, MD; Dawn Bowers, PhD; Mieke Verfaellie, PhD; Kenneth M. Heilman, MD \s=b\ Although aphasic patients with frontal lobe damage may demonstrate impaired retention of verbal material, significant anterograde memory disturbances have not, to our knowledge, been reported with a minor Broca's aphasia. We describe a patient with minor Broca's aphasia who exhibited an unusual and profound anterograde memory disturbance, especially for phonologically specified stimuli. We suggest that this disturbance is attributable to an impairment in the volitional, controlled search of stored phonological information. (Arch Neurol. 1991 ;48:949-955) number of investigators have dem"^ onstrated that anterior aphasia may be associated with impaired reten¬ tion of verbal material.1"3 Cermak and Moreines,4 for example, reported that patients with nonfluent aphasia were impaired on a phonological memory task involving the detection of rhymes; they proposed that anterior aphasia induced a defect of "phonemic recirculation." More recently, Cermak and coworkers0 have further suggested that the memo¬ ry deficits of anterior aphasies may be related to an inability to compare phono¬ logical items already in memory and dif¬ ficulty in "reconstructing" items based on phonological features. Broca's aphasia is typically associated with lesions involving Broca's area as well as portions of the anterior perisyl¬ vian region, including the sensory mo¬ tor cortex, insula, and anterior parietal operculum." Smaller lesions largely or entirely restricted to Broca's area, how¬ ever, have also been shown to be associ¬ ated with a language disturbance; this syndrome, designated minor Broca's aphasia by Foix,7 is characterized by a combination of difficulties, often includ¬ ing word-finding disturbance, effortful articulation, and decreased verbal flu¬ ency. Although sometimes initially se¬ vere, these symptoms are typically transient, and persistent, overt lan¬ guage disturbances are uncommon. Accepted for publication January 31,1991. From the Department of Neurology, Temple University School of Medicine, Philadelphia, Pa (Dr Coslett), and the University of Florida College of Medicine and the Veterans Affairs Medical Center, Gainesville, Fla (Drs Bowers, Verfaellie, and Heilman). Reprints not available. Although nonaphasic patients with left frontal lobe lesions may have lexical retrieval impairments, as evidenced by their poor performance on controlled word association tasks,8,9 to our knowl¬ edge significant anterograde memory disturbances have not been reported with a minor Broca's aphasia. We de¬ scribe a patient with minor Broca's aphasia subsequent to an ischemie in¬ farction involving Broca's area and small portions ofthe inferior and middle frontal gyri who exhibited an unusual and profound anterograde memory dis¬ turbance; we suggest that this distur¬ bance is attributable to an impairment in the volitional, controlled search of stored phonological information. REPORT OF A CASE The patient was a right-handed 59-yearold man who was admitted for evaluation of a memory impairment. He had been in excel¬ lent health until 3 years prior to admission when, 1 week after a transient episode of lefteye blindness, he noted the sudden onset of difficulty in speaking and weakness of the right side of his body. Neurologic evaluation at that time revealed a mild right hemipare¬ sis, a nonfluent aphasia with mildly impaired auditory comprehension, and a Gerstmann's syndrome. The auditory comprehension im¬ pairment and Gerstmann's syndrome re¬ solved within several days. Unfortunately, no additional information about the patient's initial language impairment is available. Although family members noted no im¬ pairment in his speech after the stroke, the patient considered himself to be appreciably less articulate because he had difficulty in finding the appropriate word and in "getting words out." In the estimation of the patient and his family, however, his subtle speech impair¬ ment paled in significance relative to the se¬ vere and disabling memory deficit noted sub¬ sequent to his stroke. Although he believed his memory for faces, pictures, and places to be relatively unimpaired, he stated that his memory for names and verbal material, whether written or spoken, was quite poor. As a consequence of his memory deficit, he was unable to return to his job as a loan officer for a finance company; he worked briefly as a prison officer before his memory disturbance forced him to retire. Neurologic examination 3 years after the stroke revealed a mild spastic weakness and clumsiness of the right hand. Evaluation of the patient's higher nervous system func¬ tions revealed that his spontaneous speech, although marked by occasional word-finding pauses, was fluent, with normal prosody and Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/11/2015 articulation. His discourse contained a nor¬ mal range of syntactic structures. Naming, although occasionally hesitant, was normal. Repetition of words, phrases, and sentences was excellent; sentences of up to 12 words, as well as sentences with unusual syntactic structures, such as center-embedded clauses, were repeated perfectly. Auditory comprehension was unimpaired. The patient read aloud and for comprehension quite well. No effect of orthographic regularity, part of speech, or imagery was noted in his reading. His writing was normal. Calculations, rightleft discrimination, and finger naming were normal. No buccofacial or limb apraxia was noted. There was no neglect. He was able to draw a cube, as well as maps of the United States. A computed tomographic scan performed 3 years after the patient's stroke revealed an old area of infarction involving Broca's areas, as well as more rostral portions ofthe inferior frontal gyrus. Additionally, small portions of the precentrai and middle frontal gyri were also infarcted (Figs 1 and 2). NEUROPSYCHOLOGICAL EVALUATION Intellectual On the Weschler Adult Intelligence Scale, the patient obtained a verbal in¬ telligence quotient (IQ) of 93, a perfor¬ mance IQ of 88, and a full-scale iQ of 91. His performance IQ was thought to have been adversely influenced by his right-hand clumsiness. The Peabody Picture Vocabulary Test10 yielded a ver¬ bal IQ estimate of 103. Language A number of formal tests were admin¬ istered for more careful assessment of the patient's language capacities. His performance on the Western Aphasia Battery11 and selected portions of the Boston Diagnostic Aphasia Examina¬ tion,12 including the reading, repetition, and writing subtests, was essentially perfect. For further assessment of the patient's auditory comprehension, the Token Test13was administered; the pa¬ tient made one mistake on subtest VI, but otherwise his performance was per¬ fect. He performed normally on the Bos¬ ton Naming Test"; the Florida Syntax Comprehension Test,15 in which correct performance is critically dependent on comprehesion of the distinction be¬ tween indirect and direct objects; and the Battery of Adult Reading Func¬ tion,16 a test that assesses reading com¬ prehension and the reading aloud of reg- Table 1.—Wechsler Memory Scale (Form I) Information Orientation Mental control Memory passages 6 Digits total 8 5 5 6 6, 4 delayed Visual reproduction Associate learning Memory quotient 1.5 71 mance was in the normal range on both tasks. Thus, the patient performed normal¬ ly on a wide range of language tasks and exhibited a normal verbal IQ. In spite of his at least relatively normal language Fig 1.—A low ventricular computed tomo¬ graphic scan image demonstrating an infarct involving the inferior frontal gyrus. Fig 2.—A high ventricular computed tomo¬ graphic scan image demonstrating an infarct involving the inferior frontal gyrus and small portions of the middle frontal gyrus. ular and irregular nouns, functors, and nonwords. The Story Completion Test" was also administered; with a single ex¬ ception, the patient generated a re¬ sponse ofthe desired syntactic form. Scale was six initially (average normal, 10) and four after a 20-minute delay (av¬ erage normal, eight). His paired-asso¬ ciate learning was similarly impaired on word-list learning tasks, both with audi¬ tory and visual presentation. On the Rey Auditory Verbal Learning Test,22 for example, he recalled no more than six of the 15 words across any of five learning trials, and his delayed 20-min¬ ute recall was three. Similar results were obtained with visual presentation. His memory performance fell more than 2 SDs below the mean of age-matched controls. The patient's performance on the Rey Auditory Verbal Learning Test also provided an opportunity for assessment of the effects of recency and primacy in supraspan list learning. On the first five trials on both the auditory and visual versions of the Rey Auditory Verbal Learning Test, the patient correctly produced 90% of the 20 items presented Frontal Lobe Tasks Several cognitive tasks sensitive to frontal lobe functioning were adminis¬ tered. The patient performed poorly on the Wisconsin Card Sorting Test18; he failed to detect the correct sorting prin¬ ciple after 35 trials. Approximately 20% of his errors were random guesses and 50% were perseverative errors. The pa¬ tient was also impaired on the colornaming and interference subtests ofthe Stroop Interference Task.19 He re¬ quired 88 seconds to name color patches (1.5 SDs below the mean) and 288 sec¬ onds to complete the interference task (2 SDs below the mean). The patient demonstrated no perseveration in Lur¬ ia's "mn" writing task but performed quite poorly on the "go-no go" and con¬ trasting motor programs task.2" Attention and Memory Digit span was assessed on a number of occasions. The patient correctly re¬ peated 100% of orally presented fivedigit lists and 60% of six-digit strings. Seventy-one percent of the errors were sequencing errors, and 29% of the er¬ rors were due to the omission of a single item. With visual presentation of singledigit written numbers at the rate of ap¬ proximately one number per second, the patient's performance was quite similar. Administration of the Wechsler Memory Scale21 revealed the patient to have a memory quotient of 71 (Table 1). His story recall of the logical memory stories from the Wechsler Memory in the last two positions. Additionally, the effects of recency and primacy were evaluated by calculation of the percent¬ age of words reported as a function of position in the list; in the first five trials on the auditory and visual versions of the test, the patient correctly reported 20% of the words from the first third, 16% ofthe words from the middle third, and 72% ofthe words from the last third ofthe list. Thus, the patient exhibited a clear effect of recency but no clear effect of primacy. In contrast, the patient performed much better on nonverbal recent memo¬ ry tasks such as the Milner Facial Rec¬ ognition Test23 and Kimura's Recurring Figures Test.24 He correctly identified nine ofthe 12 target faces and obtained a score of 44 on the latter task; his perfor- Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/11/2015 skills, however, he has a marked verbal memory deficit with sparing of nonver¬ bal memory. The following investiga¬ tions were performed to further charac¬ terize the patient's memory im¬ pairment. Rate of Forgetting.—As perfor¬ assessing the rate of for¬ mance on tests getting has been demonstrated to dis¬ tinguish between amnestic syndromes caused by bitemporal vs diencephalic damage,20"27 the patient's rate of forget¬ ting was assessed in a manner similar to that described by Huppert and Piercy.2" One hundred target stimuli (pictures) were individually projected on a screen for a period of 8 seconds each. At inter¬ vals of 10 minutes, 20 minutes, 90 min¬ utes, 24 hours, and 1 week after this presentation, different random subsets of 20 pictures from the original sample and 20 new pictures were projected, and the patient was asked to indicate wheth¬ er each picture was from the original list of stimuli. Five age- and educationmatched controls were tested in a simi¬ lar fashion, except that stimuli were presented for 1 second each. Although the difference in exposure times ren¬ ders a comparison with control subjects difficult, it is apparent from examina¬ tion of Fig 3 that the patient's perfor¬ mance was quite similar to that of five age- and education-matched controls, falling within 1 SD of their performance at every test interval. The patient's rate of forgetting for verbal stimuli was also assessed in the manner described above. Stimuli for this experiment included 100 slides de¬ picting a single typed word. The target words were presented for 8 seconds each, and the patient's recognition was assessed in the manner described above. The patient correctly sorted only 57% of the stimuli at both 10 and 20 minutes; as his performance was not above the chance level ( 2 1.63; P>. 1), this investigation was discontinued af¬ ter the second session. Errors included = . an almost equal number of false-posi¬ tives and false-negatives. With a 1-second stimulus exposure, controls cor¬ rectly identified 81% and 75% of stimuli at 10 and 20 minutes, respectively, and remained well above chance (67% cor¬ rect) after 1 week (Fig 4). Thus, the patient's rate of forgetting was essentially normal for "nonverbal" material; his rate of forgetting for ver¬ bal material could not be assessed, as we could not demonstrate evidence of ade¬ quate initial performance. Effect of Interference.—A Peterson and Peterson28 task adapted from But¬ ters and Grady29 was given to assess the effects of interference on the patient's verbal memory performance. On each trial, three semantically and phonologically unrelated monosyllabic or bisyllabic words were auditorally presented to the patient at the rate of approximately one word per second. Five trials were presented in each of four conditions: (1) immediate recall, in which there was no delay between stimulus presentation and production; (2) a 20-second unfilled delay between stimulus presentation and production, during which the pa¬ tient was permitted to rehearse; (3) a 20-second filled delay, during which the patient was asked to count backward by twos before recalling the stimuli; and (4) a 4-second unfilled interval, during which the patient was encouraged to rehearse, followed by a 16-second peri¬ od, during which the patient was asked to count backward by twos. In the im¬ mediate recall and 20-second unfilled delay conditions, the patient correctly produced all 15 ofthe target words; with a 20-second filled delay, the patient pro¬ duced only two (13%) of 15 words; with a 4-second predistractor delay, followed by a 16-second filled delay, he produced nine (60%) of 15 words (Fig 5). On the latter two conditions, errors included 16 omissions and two intrusions. No se¬ mantic errors were noted. The patient's performance was quite similar with vi¬ sual presentation of the stimuli. He made no errors in the immediate recall and unfilled delay conditions, and he correctly produced six (40%) of 15 stim¬ uli with a 20-second filled delay and pro¬ duced eight (53%) of 15 stimuli with a 4-second predistractor period and a 16-second delay and distraction. Errors included three intrusions and 13 omis¬ sions. These data suggest that the patient is quite sensitive to the effects of interfer¬ ence or, alternatively expressed, de¬ pendent on continued rehearsal. In con¬ junction with the demonstration that the patient exhibited a relatively nor¬ mal recency effect, these data suggest that rehearsal within the articulatory 10 min 20 min 90 min 24 h 1 wk Interval to Test Fig 3. —Performance of the patient and controls, expressed as percentage correct, on a test assessing the rate of forgetting of pictures. 10 min 20 min 90 min 24 h 1 wk Interval to Test Fig 4.—Similar to Fig 3 except that stimuli were words rather than pictures. NA indicates not applicable. Fig 5. —Percentage correct on a Peterson-Peterson memory task with auditory stimuli. Patient No Delay 20-s Silent Delay Conditions Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/11/2015 20-s Delay/ Distraction 4-s Predistractor Delay 100 80 8060 -Q- Patient, No Shift 40' - - Patient, Shift *- Controls, No Shift -0- Controls, Shift 20' -o- Patient -* Case Rhyme Controls Semantic Condition Fig 7. —Performance, expressed as percent¬ age correct, of the patient and controls on a level of processing task with written stimuli. ->— - 6 Trials Fig 6.—The performance of the patient and controls, expressed as percentage correct, on a release from proactive inhibition task. loop is not impaired. Release from Proactive Inhibi¬ tion.—In an attempt to assess the pos¬ sible role of impaired semantic/concep¬ tual encoding in the production of the patient's memory deficit, a releasefrom-proactive-inhibition task similar to that of Cermak et al3 was adminis¬ tered. This task was derived from Wickens'30 modification of the Peterson and Peterson28 distraction technique, in which subjects were given several con¬ secutive trials of word stimuli, all of which belonged to the same semantic category (eg, fruits). This was followed by a trial in which the word stimuli were exemplars of a different category (eg, vegetables). As previously document¬ ed, memory performance in normal sub¬ jects deteriorates over trials, because of the buildup of proactive interference. Wickens30 demonstrated, however, a dramatic improvement in memory per¬ formance on trials when the stimuli came from a different semantic catego¬ ry. This improvement presumably stemmed from a release of proactive in¬ terference that occurred because sub¬ jects had noted the change or shift in the semantic category of the stimulus words. The underlying assumption is that stimuli must be semantically en¬ coded for the release effect to occur. To assess release from proactive in¬ terference, the patient ana controls were tested on a Peterson and Peter¬ son28 distraction task involving eight blocks of five trials. Stimuli for each trial consisted of three semantically re¬ lated concrete nouns (eg, pear, apple, and grape) read aloud to the patient. After a 20-second delay filled with counting backward by twos, the patient was asked to produce the three target words. There were two conditions. In the no-shift condition, all five trials of the block consisted of word stimuli from the same semantic category (eg, fruit). In the category shift condition, word stimuli on trial 5 were from a different semantic category (eg, vegetables) than the preceding four trials of the block. Category shift and no-shift conditions were randomized, with 5-minute rest intervals between each block. The per¬ formance ofthe patient and normal con¬ trols across trials 1 through 5 of the categoryshift and no-shift conditions is shown in Fig 6. For both the patient and the controls, there was a progressive decline in performance across trials 1 through 4 of both conditions, with the patient exhibiting a greater decrement, which presumably reflects a greater susceptibility to interference. The pa¬ tient, like amnesic patients with Korsakoff's psychosis,3 exhibited no "release" effect. For controls, in contrast, the change in semantic class on trial 5 ofthe category shift condition was associated with a significant increase in recall as compared with the no-shift condition (X2 4.91;ri/=1;P<.05). = The interpretation of this finding, however, is unclear. Some investiga¬ tors3 have argued that the finding in¬ dicates that the patients were not en¬ coding in semantic categories. Alterna¬ tively, on the basis of a comparison of the performance of patients with frontal or temporal lobectomy on a releasefrom-proactive-inhibition task, Mosco¬ vitch31 has argued that the phenomenon is more appropriately associated with frontal impairment than with memory loss.32 Because our patient was impaired on tests of frontal lobe function as well as memory, the explanation for his fail¬ ure to manifest the release phenomenon is not clear. Memory for Phonology.—Levels of Processing.—Perhaps the most strik- Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/11/2015 ing aspect of the patient's verbal memo¬ ry deficit was a marked discrepancy be¬ tween performance on tasks requiring registration and/or retrieval of phonologically, compared with semantically, specified items. This phenomenon was first noted on a task employing the "lev¬ els of processing" paradigm.33 This ex¬ periment was motivated by a conceptu¬ al framework suggesting that the adequacy of memory registration is a function of the depth of analysis or the degree to which the stimulus is semanti¬ cally processed. Stimuli for this task included 36 tar¬ get words printed on a 4 x 6-in card; half of the words were printed in uppercase and half in lowercase letters. Stimuli were shown to the patient for approxi¬ mately 5 seconds each; immediately af¬ ter the presentation of each stimulus, the patient was asked one of three types of orienting questions: (1) one third of the stimuli were accompanied by ortho¬ graphic orienting questions (eg, "Is this word written in uppercase letters?"); (2) one third were accompanied by pho¬ nological orienting questions (eg, "Does this word rhyme with fear?"); and (3) one third were accompanied by se¬ mantic orienting questions (eg, "Is this a type of fruit?"). Ten minutes later, a recognition memory task was adminis¬ tered in which thirty-six 4 6-in cards, each containing one of the stimuli and three phonologically and semantically unrelated foils, were presented. The pa¬ tient was asked to indicate which of the four words had been previously presented. As depicted in Fig 7, the patient cor¬ rectly identified 87% ofthe words intro¬ duced with a semantic orienting ques¬ tion, 87% of the words introduced with an orthographic orienting question, but only 25% ofthe words introduced with a phonological orienting question. In con¬ trast, five age- and education-matched controls showed the expected pattern, correctly identifying 91% of the seman¬ tically, 75% of the phonologically, and 67% ofthe orthographically cued words. · Table 2.—Fluency Tasks Patient Controls Letters f 2.4 a 2.0 s 2.6 12.3 2.0 16.0 Semantic categories Rhyming words Nonverbal (figures) 14.5 8.4 performed in which he was asked to generate words beginning with a and s. Data were collected for each of the were Delay Trials Fig 8. —Number of rhyming and semantically related paired associates recalled by the patient with auditory and written stimuli. The patient's selective memory deficit for phonologically cued stimuli could not be attributed to an inability to make rhyme judgments, in that he was 100% accurate when answering rhyme orient¬ ing questions. An auditory version of the levels of processing task was also performed. On this task, the orthographic orienting question was eliminated, and the pa¬ tient was asked to indicate if the words were spoken in a male or female voice. The patient correctly identified 93% of the words presented with a semantic orienting question, 75% of the words introduced with a male/female voice ori¬ enting question, but only 25% of the words introduced with a phonological orienting question. Controls correctly identified 91%, 75%, and 67% of stimuli introduced with semantic, phonological, and voice orienting questions. Rhyming Paired-Associate Tasks.— The patient's apparent deficit in memo¬ ry for phonologically encoded and/or re¬ trieved information was also assessed using two list-learning tasks adapted from Warrington and Weiskranz.34 Stimuli for one task included 12 pairs of semantically related words (eg, "ask" and "inquire"); stimuli for the second task included 12 pairs of rhyming words (eg, "chair" and "bear"). The word pairs from each list were read to the patient at the rate of one word per second. After presentation of the paired-associate list, the patient was given the first word ofthe pair and asked to produce its asso¬ ciate. This procedure was repeated for a total of four trials for each of the two lists. Delayed recall of the word pairs was tested after a 30-minute delay. The semantically and phonologically related word pairs were presented in different sessions. Both visual and auditory ver¬ sions of these lists were given. The patient's performance with writ¬ ten and auditory stimuli presentation is presented in Fig 8. He performed better with semantically related stimuli on each trial with both written and audi¬ tory stimuli. With written stimuli, this difference reached significance on trials 2, 3, and 4 ( 2 6.3, 8.7, 12.0, respec¬ tively; all P<.01). With auditory stimu¬ li, he performed significantly better with semantically related pairs on trials 3 and 4 (x2 10.7and 8.2, respectively; both P<.05). Summing across the five trials, the patient performed signifi¬ cantly better with semantic, as com¬ pared with rhyming, paired associates with both written ( 2 30.0; P<. 01) and auditory ( 2 17.7; P<.01) stimuli. Age- and education-matched controls demonstrated no significant difference between rhyming and semantically as¬ sociated words on individual trials but did demonstrate a slight but consistent superiority with semantic paired asso¬ ciates which, summing over all five tri¬ = = = = als, was significant ( 2 5.6; P<.05). Fluency Tasks.—The effect of pho¬ nological factors on retrieval of informa¬ tion from remote or long-term memory was assessed by a number of variants of the Thurstone Word Fluency Test3,5 (Ta¬ ble 2). In one investigation, the patient's ability to generate words beginning with a designated letter was compared with his ability to generate words de¬ = fined on the basis of semantic attri¬ butes. In the former task, the patient was instructed to generate in 1 minute as many words as possible that begin with the letter/; similar 1-minute trials Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/11/2015 three letters during five separate ses¬ sions. The patient was also instructed to generate in 1 minute as many exemplars as possible of a specified semantic cate¬ gory. Eight semantic categories were tested on each of two occasions. As indicated in Table 2, the patient's average score for the letters f a, and s was 2.4, 2.0, and 2.6 words per minute, respectively; thus, his average across all three letters was 2.3 words per min¬ ute. Performance with semantically de¬ fined categories was substantially bet¬ ter, as he generated an average of 12.3 items per minute, with a range of 6 to 18. On another occasion, a word was pro¬ vided, and the patient was asked to gen¬ erate as many rhyming words as possi¬ ble in 1 minute. A total of five words were presented. He produced an aver¬ age of 2.0 rhyming words per minute; he did not produce nonrhyming words. Age- and education-matched controls, in contrast, generated an average of 8.4 words per minute. In an effort to demonstrate that the diminished fluency reflected a specifi¬ cally verbal impairment, a nonverbal analog of the Thurstone Word Fluency Test was administered in which the pa¬ tient was asked to create as many differ¬ ent drawings in 4 minutes as possible using only four lines.36 On two trials he created an average of 16 drawings, a performance that is within the normal range. COMMENT We have presented data derived from 59-year-old man with a minor Broca's aphasia secondary to a documented left a dorsolateral frontal lobe infarct who demonstrated a severe memory impair¬ ment of a type not previously described, to our knowledge. Evaluation ofthe pa¬ tient's memory revealed that he was sensitive to distraction, did not demon¬ strate the normal release from proac¬ tive inhibition, showed an effect of re¬ cency but not primacy, and, perhaps most interestingly, exhibited a marked memory impairment for the encoding and/or retrieval of phonologically, com- with semantically, specified items. Several issues concerning this patient's performance warrant atten¬ tion. The first issue concerns the relation¬ ship between the patient's language ca¬ pacities and his memory impairment. Abundant evidence suggests that both fluent and nonfluent aphasias may be associated with a verbal memory im¬ pairment. Might the patient's memory deficit be secondary to a subtle language deficit? A number of specific mechanisms have been proposed to account for the impairments of short-term memory en¬ countered in aphasie patients. The im¬ paired verbal short-term memory en¬ countered in a probable Wernicke aphasie, for example, has been attribut¬ ed to a failure to generate an adequate phonological representation37; the im¬ pairment seen in certain conduction aphasies has been attributed to a patho¬ logic reduction in the capacity of the short-term store38,39; finally, in certain Broca's aphasies, the impairment of short-term memory has been attributed to failure of repetition, with a resultant failure of rehearsal in the putative artic¬ pared ulatory loop.18,40 None of these proposed explanations, however, can account for the data de¬ rived from our patient. Our patient ex¬ hibited no demonstrable phonological impairment on tests of auditory com¬ prehension, phoneme discrimination, and rhyme judgment. Additionally, our patient had no impairment of repetition and, as indicated by his perfect perfor¬ mance on the Peterson and Peterson28 task with an unfilled delay, was able to retain phonologically encoded data, pre¬ sumably by means of rehearsal within the articulatory loop. Because the patient's infarct involves Broca's area, a brain region thought to be important in the control of motor aspects of speech production, one might suggest that the memory deficit reflects an impairment at the level of motor pro¬ gramming for speech. There are several lines of evidence that make this possibil¬ ity seem unlikely. The patient's sponta¬ neous speech demonstrates only a mini¬ mal abnormality—occasional wordfinding problems—that might be attributed to an impairment of the mo¬ tor programmer. Additionally, this hy¬ pothesis provides no principled account ofthe dissociation between the retrieval of phonologically, compared with se¬ mantically, guided retrieval. Finally, a deficit with phonologically cued stimuli was documented on the levels of pro¬ cessing task in which no verbal output was necessary. A second issue concerns the marked dissociation between the patient's nor¬ mal phonological processing in natural¬ istic, "automatic" language tasks such as spontaneous speech, reading, and naming and his marked impairment on memory and fluency tasks requiring the strategically guided, "controlled" re¬ trieval of phonologically specified items. Following Schneider and Shiffrin41 and Shiffrin and Schneider42, a con¬ trolled process refers to an attentionrequiring procedure that may be accessed or developed for the comple¬ tion of a novel or unusual task. Tasks such as the production of lists of rhym¬ ing words that are not part of normal language routines may require a strate¬ gically guided or controlled search of lexical phonology. An automatic pro¬ cess, in contrast, is effortless and pro¬ ceeds without active control; the seman¬ tically guided activation of lexical phonology that is thought to character¬ ize normal routines involved in speech production43 and object naming may in¬ volve an automatic process. Within this framework, one possible explanation for the patient's deficits is an impairment in the controlled search of stored information. This hypothesis may take at least two forms. First, one might propose that the deficit is specific to the domain of lexical phonology; in this hypothesis, the controlled search of lexical semantics is assumed to be nor¬ mal. Because tasks such as the retrieval of phonology on the basis of rhyme or initial letter are assumed to require con¬ trolled search of phonological informa¬ tion, whereas spontaneous speech, naming repetition, and reading are as¬ sumed to be mediated by the relatively automatic procedures involved in nor¬ mal speech production, this hypothesis for the can account patient's performance. A second explanation is that the pa¬ tient suffers from a general impairment in controlled search. On this hypothesis, the difference in performance between phonologically and semantically speci¬ fied items might reflect differences in the amount of effort required for con¬ trolled searches of the semantic and phonological stores, which, in turn, may reflect discrepancies in the organization of these stores; an impaired procedure for controlled search may be more effec¬ tive operating within the semantic do¬ main, in which related items may be "linked," compared with phonological stores, in which such interrelationships are weak or absent. One might expect, for example, that the retrieval of animal names would be facilitated by the multi¬ plicity of semantic and, perhaps, visual attributes that they share; in contrast, preexisting linkages between words Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/11/2015 sharing an initial letter in the phonologi¬ cal lexicon would be expected to be weak. The hypothesis that the patient's symptoms reflect an impairment in con¬ trolled search of stored information also accounts for another interesting aspect of his performance: the relatively nor¬ mal recency effect, but the failure to demonstrate primacy. Recency effects are typically attributed to the mainte¬ nance of phonological information in the articulatory loop or phonemic buffer; primacy effects, in contrast, are typical¬ ly attributed to the activation of lexical information. Thus, the ability to pro¬ duce words from the beginning of a list (ie, primacy) may require the controlled search of lexical phonology, which, in our hypothesis, is assumed to be impaired. Anatomic studies in monkeys provide data consistent with the proposal that the patient's dorsolateral frontal lobe infarct is associated with a defect in the controlled search of lexical phonology. Chavis and Pandya,44 for example, dem¬ onstrated that the frontal lobes (includ¬ ing the dorsolateral, medial, and orbito¬ frontal portions) have reciprocal connections with the primary auditory and auditory association cortex. One might speculate that the left dorsolater¬ al frontal lobe plays a critical role in the retrieval of lexical phonology by virtue of its role in the activation of the audi¬ tory association cortex (including Wer¬ nicke's area), which may support lexical phonology in man. An important, but thus far unan¬ swered, question is whether the puta¬ tive deficit in controlled search under¬ lies the patient's memory impairment. Although one might expect a general deficit in controlled search of stored in¬ formation to cause a memory impair¬ ment, in the absence of an explicit ac¬ count of the role of phonological factors in encoding and retrieval, it is not clear whether a specific impairment in the retrieval of phonologically specified in¬ formation would cause amnesia. It is also possible, of course, that the impair¬ ment in controlled search and memory deficit are unrelated but co-occur be¬ cause both processes are dependent on structures in the left dorsolateral fron¬ tal lobe. An additional issue concerns the im¬ plications of our patient's performance for conceptions regarding the relation¬ ship between the frontal lobe and mem¬ ory. Investigations involving mon¬ keys45,46 and man47,48 have suggested that frontal lobe damage may be associated with specific memory impairments. Other researchers, however, have ar¬ gued that the apparent memory failure observed with frontal lobe damage does not represent a specific impairment of encoding or retrieval but a disruption of more complex forms of human behav¬ ior.9,29 Luria,49 for example, argued that patients with frontal lobe damage are unable to maintain a stable intention to remember and are plagued by "patho¬ logic inertia" and "high distractibility." In a similar vein, Warrington and Weiskranz34 proposed that the frontal lobes play a critical role in the cognitive mediation mechanism, which serves to organize, manipulate, and embellish memory input. Signoret and Lher¬ mitte0" provided empirical support for the proposal that memory deficits asso¬ ciated with frontal lobe damage may be related to a deficit in the organization of material to be learned, rather than en¬ coding or retrieval per se; these investi¬ gators described two patients with fron¬ tal lobe damage who were severely impaired in paired associate list learn¬ ing but were relatively unimpaired when the stimuli were presented in a sentence context or with instructions to generate a visual image of the named objects. Although the data derived our pa¬ tient confirm previous observations that even relatively minor frontal lobe damage may be associated with a pro¬ found memory impairment, these data do not permit one to adjudicate between these possibilities. To the extent that the memory impairment is attributable to the putative deficit in controlled search of lexical phonology, the data support the thesis that frontal lobe am¬ nesia is attributable to higher-level im¬ pairments rather than to impaired en¬ coding or retrieval. Alternatively, ifthe memory deficit and impairment in con¬ trolled search are unrelated, the data may be consistent with the view that the frontal lobes are critical for encoding and/or retrieval. Finally, one might wonder why the at least relatively selective impairment in processing of phonologically cued infor¬ mation demonstrated by our patient has not been reported previously. 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