A positron emission tomography study of the short-term maintenance of verbal information

Positron emission tomography (PET) was used to investigate the functional brain anatomy associated with the short-term maintenance of linguistic information. Subjects were asked to retain five related words, unrelated words, or pseudowords silently for the duration of a 40 sec PET scan. When brain activity during these short-term maintenance tasks was compared with a visual fixation control task, increases were found bilaterally in the dorsolateral prefrontal cortex and cerebellum, and medially in the supplementary motor area. Furthermore, effects of stimulus condition and recall performance were found in the left frontal operculum. To investigate the role of articulatory systems in the maintenance of verbal information, regional activation was compared across the maintenance tasks and a covert articulation task (silent counting). The cerebellum was active in both task conditions, whereas activation in prefrontal regions was specific to the maintenance condition. Conversely, greater activation was found in a left middle insular region in the silent counting than in the maintenance tasks. Based on converging results in this and previous studies, dorsolateral prefrontal cortical areas appear to contribute to the maintenance of both verbal and nonverbal information, whereas left frontal opercular regions appear to be involved specifically in the rehearsal of verbal material. Contrary to results found in other studies of working memory, activation was not found in the inferior parietal cortex, suggesting that this area is involved in aspects of stimulus encoding and retrieval, which were minimized in the present study.

[1]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[2]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[3]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Corballis,et al.  Effects of concurrent memory load on visual-field differences in mental rotation , 1993, Neuropsychologia.

[5]  Gordon D. A. Brown,et al.  Memory for familiar and unfamiliar words: Evidence for a long-term memory contribution to short-term memory span , 1991 .

[6]  M. E. Raichle,et al.  PET Studies of Auditory and Phonological Processing: Effects of Stimulus Characteristics and Task Demands , 1995, Journal of Cognitive Neuroscience.

[7]  P T Fox,et al.  A Highly Accurate Method of Localizing Regions of Neuronal Activation in the Human Brain with Positron Emission Tomography , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[8]  M. Mintun,et al.  Noninvasive functional brain mapping by change-distribution analysis of averaged PET images of H215O tissue activity. , 1989, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[9]  M. Mintun,et al.  Enhanced Detection of Focal Brain Responses Using Intersubject Averaging and Change-Distribution Analysis of Subtracted PET Images , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[10]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[11]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[12]  J. Fuster The Prefrontal Cortex , 1997 .

[13]  P S Goldman-Rakic,et al.  Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria. , 1995, Cerebral cortex.

[14]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[15]  Bart Rypma,et al.  Age differences in components of mental-rotation task performance , 1991 .

[16]  R. Nebes,et al.  Reliability and validity of some handedness questionnaire items. , 1974, Neuropsychologia.

[17]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Raichle,et al.  A Stereotactic Method of Anatomical Localization for Positron Emission Tomography , 1985, Journal of computer assisted tomography.

[19]  Alan B. Welsh,et al.  Acoustic masking in primary memory. , 1976 .

[20]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  H. Spinnler The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

[22]  S. Wise,et al.  The premotor cortex of the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Randy L. Buckner,et al.  Neuroimaging Studies of Memory: Theory and Recent PET Results , 1995 .

[24]  Peter Herscovitch,et al.  Brain blood flow measured with intravenous H/sub 2//sup 15/O. I. Theory and error analysis , 1983 .

[25]  J. Decety,et al.  Brain structures participating in mental simulation of motor behavior: a neuropsychological interpretation. , 1990, Acta psychologica.

[26]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[27]  J. Fuster Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[28]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[29]  P. Casey “That man’s father is my father’s son”: The roles of structure, strategy, and working memory in solving convoluted verbal problems , 1993, Memory & cognition.

[30]  P. Goldman-Rakic,et al.  The Issue of Memory in the Study of Prefrontal Function , 1994 .

[31]  B. J. Casey,et al.  Activation of the prefrontal cortex in a nonspatial working memory task with functional MRI , 1994, Human brain mapping.

[32]  N Cowan,et al.  Implications of aging, lexicality, and item length for the mechanisms underlying memory span , 1996, Psychonomic bulletin & review.

[33]  D. V. van Essen,et al.  Retinotopic organization of human visual cortex mapped with positron- emission tomography , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  D. J. Murray Articulation and acoustic confusability in short-term memory. , 1968 .

[35]  J. Fuster Prefrontal Cortex , 2018 .

[36]  S J McCrory,et al.  Statistical Issues in the Analysis of Neuroimages , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[37]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[38]  D. Hoffman,et al.  Differential effects of muscimol microinjection into dorsal and ventral aspects of the premotor cortex of monkeys. , 1994, Journal of neurophysiology.

[39]  An Assessment of Replication and Functional-anatomical Variability in Functional Neuroimaging Studies , 1996 .

[40]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[41]  J. Decety,et al.  The cerebellum participates in mental activity: tomographic measurements of regional cerebral blood flow , 1990, Brain Research.

[42]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[43]  R S Frackowiak,et al.  A PET study of cognitive strategies in normal subjects during language tasks. Influence of phonetic ambiguity and sequence processing on phoneme monitoring. , 1994, Brain : a journal of neurology.

[44]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[45]  P. Goldman-Rakic,et al.  Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach Coordinate System. , 1995, Cerebral cortex.

[46]  M. Welch,et al.  A remote system for the routine production of oxygen‐15 radiopharmaceuticals , 1985 .

[47]  Cheryl L. Grady,et al.  Hemispheric differences in neural systems for face working memory: A PET‐rCBF study , 1995 .

[48]  R H Logie,et al.  Counting on working memory in arithmetic problem solving , 1994, Memory & cognition.

[49]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

[50]  M. Just,et al.  From the SelectedWorks of Marcel Adam Just 1992 A capacity theory of comprehension : Individual differences in working memory , 2017 .

[51]  M. Ter-pogossian,et al.  PETT VI: A Positron Emission Tomograph Utilizing Cesium Fluoride Scintillation Detectors , 1982, Journal of computer assisted tomography.

[52]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  W. Montague,et al.  Category norms of verbal items in 56 categories A replication and extension of the Connecticut category norms , 1969 .

[54]  G. A. Miller THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[55]  David C. Geary,et al.  Cognitive Addition : A Short Longitudinal Study of Strategy Choice and Speed-of-Processing Differences in Normal and Mathematically Disabled Children , 1991 .

[56]  Karl J. Friston,et al.  Functional mapping of brain areas implicated in auditory--verbal memory function. , 1993, Brain : a journal of neurology.

[57]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[58]  P. Goldman-Rakic,et al.  Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Edward Awh,et al.  Spatial versus Object Working Memory: PET Investigations , 1995, Journal of Cognitive Neuroscience.