PET studies on the memory processing of word pairs in bilingual Finnish–English subjects

This study examined the fundamental question whether verbal memory processing in two unrelated languages is mediated by a common neural system or by distinct cortical areas. Ten right-handed, male Finnish--English adult late bilinguals who had acquired the second language after the age of 10 were scanned whilst either encoding/retrieving word pairs in their mother tongue (Finnish) or in a foreign language (English). Within each language, subjects had to encode and retrieve four sets of 12 visually presented paired word associates which were not semantically related. Two sets consisted of highly imageable words (e.g. monkey-table; koira-lasi) and the other two sets of abstract word pairs (e.g. freedom-moral; uhka-suure). Presentation of pseudowords served as a reference condition. An emission scan was recorded after each intravenous administration of O-15 water. Encoding was associated with prefrontal and hippocampal activation. During memory retrieval, precuneus showed a consistent activation in both languages and for both highly imageable and abstract words. Although the brain mechanisms of the two languages share common components, differential activations were found in Broca's area and in the cerebellum as well as in the angular/supramarginal gyri according to the language used.

[1]  Karl J. Friston,et al.  A PET study of word finding , 1991, Neuropsychologia.

[2]  S. Kosslyn,et al.  Functional Anatomy of High-Resolution Visual Mental Imagery , 2000, Journal of Cognitive Neuroscience.

[3]  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.

[4]  U. Bellugi,et al.  Neural Systems Mediating American Sign Language: Effects of Sensory Experience and Age of Acquisition , 1997, Brain and Language.

[5]  A. Paivio,et al.  Concreteness, imagery, and meaningfulness values for 925 nouns. , 1968, Journal of experimental psychology.

[6]  S Dehaene,et al.  Electrophysiological evidence for category-specific word processing in the normal human brain. , 1995, Neuroreport.

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

[8]  Lars Nyberg,et al.  Brain Regions Differentially Involved in Remembering What and When: a PET Study , 1997, Neuron.

[9]  Michel Paradis,et al.  Generalizable Outcomes of Bilingual Aphasia Research , 1999, Folia Phoniatrica et Logopaedica.

[10]  S. Petersen,et al.  Impaired non-motor learning and error detection associated with cerebellar damage. A single case study. , 1992, Brain : a journal of neurology.

[11]  A. Paivio,et al.  Stimulus and response abstractness, imagery, and meaningfulness, and reported mediators in paired-associate learning. , 1966, Canadian journal of psychology.

[12]  H B PRIBRAM,et al.  Further behavioral analysis of parieto-temporo-preoccipital cortex. , 1956, Journal of neurophysiology.

[13]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[14]  D. Schmidt,et al.  Neuronal correlates of encoding and retrieval in episodic memory during a paired-word association learning task: a functional magnetic resonance imaging study , 1999, Experimental Brain Research.

[15]  J. Hyönä,et al.  A neurolinguistic analysis of morphological deficits in a Finnish-Swedish bilingual aphasic , 1994 .

[16]  K H PRIBRAM,et al.  A behavioral analysis of the organization of the parieto‐temporo‐preoccipital cortex , 1950, The Journal of comparative neurology.

[17]  B. Milner,et al.  Frontal lobes and the temporal organization of memory. , 1985, Human neurobiology.

[18]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

[19]  H. Müller-Gärtner,et al.  Encoding and retrieval in declarative learning: a positron emission tomography study , 1998, Behavioural Brain Research.

[20]  H. Neville,et al.  Fractionating language: different neural subsystems with different sensitive periods. , 1992, Cerebral cortex.

[21]  C. Crouzel,et al.  Current methodology for oxygen-15 production for clinical use. , 1987, International journal of radiation applications and instrumentation. Part A, Applied radiation and isotopes.

[22]  D. Wechsler A Standardized Memory Scale for Clinical Use , 1945 .

[23]  S. Dehaene,et al.  Anatomical variability in the cortical representation of first and second language , 1997, Neuroreport.

[24]  P. Goldman-Rakic,et al.  The anatomy of dopamine in monkey and human prefrontal cortex. , 1992, Journal of neural transmission. Supplementum.

[25]  Thomas K. Lewellen,et al.  Investigation of the performance of the General Electric Advance positron emission tomograph in 3D mode , 1995 .

[26]  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 .

[27]  D. Schacter Memory, amnesia, and frontal lobe dysfunction , 1987, Psychobiology.

[28]  M. Moscovitch Memory and Working-with-Memory: A Component Process Model Based on Modules and Central Systems , 1992, Journal of Cognitive Neuroscience.

[29]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[30]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[31]  Alan C. Evans,et al.  Left putaminal activation when speaking a second language: evidence from PET. , 1994, Neuroreport.

[32]  Gary H. Glover,et al.  Convergent Cortical Representation of Semantic Processing in Bilinguals , 1999, Brain and Language.

[33]  R W Cox,et al.  Use of functional MR to map language in multilingual volunteers. , 1996, AJNR. American journal of neuroradiology.

[34]  H. Müller-Gärtner,et al.  Brain systems engaged in encoding and retrieval of word-pair associates independent of their imagery content or presentation modalities , 2002, Neuropsychologia.

[35]  D L Schacter,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Medial Blockintemporal Blockinlobe Blockinactivation Blockinduring Blockinepisodic Encoding Blockinand Blockinretrieval: Blockina Blockinpet Blockinstudy , 2022 .

[36]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

[37]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Matti Laine,et al.  Left hemisphere activation during processing of morphologically complex word forms in adults , 1999, Neuroscience Letters.

[39]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[40]  F Pulvermüller,et al.  Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses. , 1999, Cerebral cortex.

[41]  R. Buckner Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval , 1996, Psychonomic bulletin & review.

[42]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Hanna Damasio,et al.  Premotor and Prefrontal Correlates of Category-Related Lexical Retrieval , 1998, NeuroImage.

[44]  V Bettinardi,et al.  The bilingual brain. Proficiency and age of acquisition of the second language. , 1998, Brain : a journal of neurology.

[45]  J. Hirsch,et al.  Distinct cortical areas associated with native and second languages , 1997, Nature.

[46]  Stephen M Kosslyn,et al.  Deficits in visual cognition and attention following bilateral anterior cingulotomy , 2001, Neuropsychologia.

[47]  J G Taylor,et al.  Network analysis in episodic encoding and retrieval of word‐pair associates: a PET study , 1999, The European journal of neuroscience.

[48]  J. Taylor,et al.  Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. , 1999, Brain : a journal of neurology.

[49]  Richard D. Hichwa,et al.  A neural basis for lexical retrieval , 1996, Nature.

[50]  Endel Tulving,et al.  Prefrontal cortex and episodic memory retrieval mode. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[52]  R. Myers Quantification of brain function using PET , 1996 .

[53]  G. Ojemann Cortical organization of language , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  S. Petersen,et al.  Activation of extrastriate and frontal cortical areas by visual words and word-like stimuli. , 1990, Science.

[55]  Guylaine Le Dorze,et al.  Bilingual Aphasia: Semantic Organization, Strategy Use, and Productivity in Semantic Verbal Fluency , 1998, Brain and Language.

[56]  Emmanuel Dupoux,et al.  Brain processing of native and foreign languages. , 1996 .

[57]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[58]  J. Fuster Memory in the cerebral cortex , 1994 .

[59]  E Tulving,et al.  Functional role of the prefrontal cortex in retrieval of memories: a PET study , 1995, Neuroreport.

[60]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[61]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[62]  Elizabeth K. Warrington,et al.  Amnesia: A disconnection syndrome? , 1982, Neuropsychologia.

[63]  P. Goldman-Rakic Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[64]  H A Whitaker,et al.  The bilingual brain. , 1978, Archives of neurology.

[65]  H. Neville,et al.  Maturational Constraints on Functional Specializations for Language Processing: ERP and Behavioral Evidence in Bilingual Speakers , 1996, Journal of Cognitive Neuroscience.

[66]  A W Toga,et al.  Optical imaging of bilingual cortical representations. Case report. , 2000, Journal of neurosurgery.

[67]  B. Rockstroh,et al.  The cerebellum contributes to mental skills. , 1989 .

[68]  E. Ross,et al.  Left medial parietal lobe and receptive language functions , 1980, Neurology.

[69]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[70]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[71]  R. Dolan,et al.  Dissociable Temporal Lobe Activations during Emotional Episodic Memory Retrieval , 2000, NeuroImage.

[72]  Nader Pouratian,et al.  Optical imaging of bilingual cortical representations , 2000, NeuroImage.

[73]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[74]  F. Fabbro The neurolinguistics of bilingualism , 1999 .

[75]  D Klein,et al.  Cerebral organization in bilinguals: a PET study of Chinese-English verb generation. , 1999, Neuroreport.

[76]  Alan C. Evans,et al.  The neural substrates underlying word generation: a bilingual functional-imaging study. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[77]  C. Price,et al.  A functional imaging study of translation and language switching. , 1999, Brain : a journal of neurology.

[78]  W H Theodore,et al.  Functional mapping of human memory using PET: comparisons of conceptual and perceptual tasks. , 1996, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[79]  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.