Semantic Encoding and Retrieval in the Left Inferior Prefrontal Cortex: a Functional MRI Study of Task Difficulty and Process Specificity
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The Journal of Neuroscience, September 1995, 15(g): 5870-5878 Semantic Encoding and Retrieval in the Left Inferior Prefrontal Cortex: A Functional MRI Study of Task Difficulty and Process Specificity Jonathan B. Demb,’ John E. Desmond,2 Anthony D. Wagner,’ Chandan J. Vaidya,’ Gary H. Glover,2 and John D. E. Gabriel? Departments of ‘Psychology and ‘Radiology, Stanford University, Stanford, California 94305-2130 Prefrontal cortical function was examined during semantic Lockhart, 1972). Retrieval refers to the recovery of previously encoding and repetition priming using functional magnetic encoded information from long-term memory and can be mea- resonance imaging (fMRI), a noninvasive technique for lo- sured explicitly, by measuresof intentional recollection, or im- calizing regional changes in blood oxygenation, a correlate plicitly, by measuresof priming, conditioning, or skill learning of neural activity. Words studied in a semantic (deep) en- (Graf and Schacter, 198.5).Priming reflects experience-basedfa- coding condition were better remembered than words stud- cilitation in performance with a stimulus that does not depend ied in both easier and more difficult nonsemantic (shallow) on intentional recollection. For example, subjects make a se- encoding conditions, with difficulty indexed by response mantic encoding decision (e.g., is this word abstract‘?)more time. The left inferior prefrontal cortex (LIPC) (Brodmann’s quickly for a repeated than an initial presentation of a word areas 45, 46, 47) showed increased activation during se- (Gabrieli, Desmond,Demb, Wagner, Stone, Vaidya, and Glover, mantic encoding relative to nonsemantic encoding regard- unpublishedobservations). less of the relative difficulty of the nonsemantic encoding Functional magnetic resonanceimaging (fMR1) and positron task. Therefore, LIPC activation appears to be related to emissiontomography (PET) studieshave indicated left inferior semantic encoding and not task difficulty. Semantic encod- prefrontal cortex (LIPC) involvement in semanticencoding. The ing decisions are performed faster the second time words LIPC area (Brodmann’s areas 45, 46, 47), anterior to Broca’s are presented. This represents semantic repetition priming, area, showsgreater activation during semanticthan nonsemantic a facilitation in semantic processing for previously encod- encoding (Gabrieli et al., unpublishedobservations; seeTulving ed words that is not dependent on intentional recollection. et al., 1994). In these studies,the semanticencoding tasks have The same LIPC area activated during semantic encoding been more difficult than nonsemanticencoding tasks, with dif- showed decreased activation during repeated semantic en- ficulty operationalized as the time required to perform an en- coding relative to initial semantic encoding of the same coding task. This difference in difficulty hasbeen shown directly words. This decrease in activation during repeated encod- in two studies(Gabrieli et al., unpublishedobservations; Kapur ing was process specific; it occurred when words were se- et al., 1994) and is likely to be the case in others. One goal of mantically reprocessed but not when words were nonse- the current study was to compare a semanticencoding task to mantically reprocessed. The results were apparent in both both less and more difficult nonsemanticencoding tasks, to in- individual and averaged functional maps. These findings vestigate whether LIPC activation reflects semanticencoding or suggest that the LIPC is part of a semantic executive sys- encoding difficulty. If LIPC activation reflects semanticencod- tem that contributes to the on-line retrieval of semantic in- ing, it should be present during the semanticencoding task rel- formation. ative to both lessand more difficult nonsemanticencoding tasks. [Key words: functional magnetic resonance imaging The sameLIPC area that activates during semanticencoding (fMR/), prefrontal cortex, semantic memory, implicit mem- has also been implicated in semanticrepetition priming. When ory, area 8, executive functioning] words were semantically encodedmore than once, subjectsen- coded more quickly the second time (priming). There was a Encoding and retrieval constitute two discrete stagesof memory. correspondingdecrease in LIPC activation for repeated relative Encoding refers to the processesoperating at the time of learning to initial semanticencoding (Gabrieli et al., unpublishedobser- that determine what information is stored in long-term memory. vations; Raichle et al., 1994). The decreasesin responsetime Different kinds of encoding lead to different kinds of storage. and brain activation representa word-specific effect; when novel For example, words are typically better rememberedwhen en- words were semantically encoded, behavioral responsesand coded for meaning (semantic or “deep” encoding) rather than LIPC activation returned to initial levels (Gabrieli et al., unpub- for appearance(nonsemantic or “shallow” encoding) (Craik and lished observations; Raichle et al., 1994). However, it is un- known whether decreasedLIPC activation reflects a process- Received Jan. 17, 1995; revised May 5, 1995; accepted May IO, 1995. specific change based on semanticreencoding, or rather a pro- This work was supported by research grants from the Stanford University cessnonspecific change based on reexposureto words regardless Office of Technology and Licensing, the Alzheimer’s Association (Blum-Kov- of the encoding processengaged. Therefore, a secondgoal was ler Pilot Research Grant), and the NIH (NINDS lF32NS09628). Correspondence should be addressed to Jonathan Demb at the above address. to clarify the nature of the decreasedLIPC activation during Copyright 0 1995 Society for Neuroscience 0270-6474/95/l 55870-09$05.00/O repeatedsemantic encoding. If decreasedLIPC activation is spe- The Journal of Neuroscience, September 1995, 15(Q) 5871 no more than four ascending or descending words appeared consecu- tively. Procedure. Each subject performed two encoding experiments. Both experiments compared a semantic encoding task, in which subjects had to decide whether words were abstract or concrete (Abstract/Concrete Task), with a nonsemantic encoding task. In the first experiment, sub- jects alternately performed the semantic encoding task and a nonse- mantic encoding task, in which subjects had to decide if words were printed in uppercase or lowercase letters (Uppercase/Lowercase Task). In the second experiment, subjects alternately performed the semantic encoding task and a nonsemantic encoding task, in which subjects had to decide if the tirst and last letter of each word were ascending or descending alphabetically (Ascending/Descending Task). The semantic encoding task required that subjects attend to word meaning, whereas both nonsemantic encoding tasks required that subjects attend to word features (i.e., letters). Subjects saw four sets of 20 words presented consecutively. One encoding task was performed on the first and third set and another task was performed on the second and fourth set. Each pair of tasks consti- tuted a cycle, so that two cycles were performed by each subject in each experiment. An instruction card at the beginning of each set of 20 Figure I. The location of the coronal slices analyzed in this study are words (e.g., Task-Abstract) indicated the target for that set (e.g., abstract depicted as white lines on a sagittal localizer. The slices shown are 32 words). Subjects were instructed to respond as quickly and as accurately and 39 mm rostra1 to the anterior commissure (AC).‘An additional third as possible to the indicated target by pressing a mouse button; they slice, 46 mm rostra1 to the AC was acquired in three subjects in the were instructed to not respond to nontarget words. Words appeared cen- Process Specificity study (see Table I). trally on a computer monitor for a duration of 1 set, followed by a 1 set interval before the next word appeared. For each task, half of the subjects responded to one kind of target (e.g., abstract or uppercase or cific to semantic processes, it should occur during repeated se- ascending) and half the subjects responded to the other kind of target mantic encoding but not during repeated nonsemantic encoding. (e.g., concrete or lowercase or descending). Word orders were kept con- stant across subjects, but the order of alternating encoding tasks was Materials and Methods counterbalanced across subjects. Thus, encoding tasks and responses were counterbalanced across words. After each experiment, subjects Behaviorul study were given a recognition test, composed of 20 studied words, half of The purpose of the behavioral study was to validate a difficult nonse- which were presented in the Abstract/Concrete Task and half of which mantic encoding condition to be used in the Task Difficulty fMR1 ex- were presented in either the Uppercase/Lowercase Task or the Ascend- periment. We predicted that this task would be more difficult than se- ing/Descending Task, and 20 new (foil) words in a random order. Words mantic encoding (longer response time; RT), but would still lead to appeared one at a time on a computer monitor and subjects were in- lower subsequent memory performance than semantic encoding. structed to respond by pressing a mouse button if they thought the Subjects. The subjects were 16 volunteers from the Stanford com- words had been in the study list. Different foil words were used after munity (ages 18-24) who participated for a $10 payment. All subjects each encoding experiment,