Neural networks for short-term memory for order differentiate high and low proficiency bilinguals

Short-term memory (STM) for order information, as compared to STM for item information, has been shown to be a critical determinant of language learning capacity. The present fMRI study asked whether the neural substrates of order STM can serve as markers for bilingual language achievement. Two groups of German-French bilinguals differing in second language proficiency were presented STM tasks probing serial order or item information. During order STM but not item STM tasks, the high proficiency group showed increased activation in the lateral orbito-frontal and the superior frontal gyri associated with updating and grouped rehearsal of serial order information. Functional connectivity analyses for order encoding showed a functional network involving the left IPS, the right IPS and the right superior cerebellum in the high proficiency group while the low proficiency group showed enhanced connectivity between the left IPS and bilateral superior temporal and temporo-parietal areas involved in item processing. The present data suggest that low proficiency bilinguals activate STM networks for order in a less efficient and differentiated way, and this may explain their poorer storage and learning capacity for verbal sequences.

[1]  H. Neville,et al.  Sensitive periods differentiate processing of open- and closed-class words: an ERP study of bilinguals. , 2001, Journal of speech, language, and hearing research : JSLHR.

[2]  Hermann Ackermann,et al.  The contribution of the insula to motor aspects of speech production: A review and a hypothesis , 2004, Brain and Language.

[3]  Ray Johnson,et al.  Lexical Contributions to Retention of Verbal Information in Working Memory: Event-Related Brain Potential Evidence , 1999 .

[4]  Karl J. Friston,et al.  Distribution of cortical neural networks involved in word comprehension and word retrieval. , 1991, Brain : a journal of neurology.

[5]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Steve Majerus,et al.  Relations between vocabulary development and verbal short-term memory: The relative importance of short-term memory for serial order and item information. , 2006, Journal of experimental child psychology.

[7]  J. Desmond,et al.  Lobular Patterns of Cerebellar Activation in Verbal Working-Memory and Finger-Tapping Tasks as Revealed by Functional MRI , 1997, The Journal of Neuroscience.

[8]  M. Poirier,et al.  Immediate serial recall, word frequency, item identity and item position. , 1996, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[9]  D. Speelman,et al.  The organisation of the bilingual lexicon: a PET study , 2003, Journal of Neurolinguistics.

[10]  Daryl Fougnie,et al.  Visual short-term memory load induces inattentional blindness , 2010 .

[11]  G D Brown,et al.  Oscillator-based memory for serial order. , 2000, Psychological review.

[12]  E. Vogel,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004 .

[13]  A. Baddeley,et al.  The phonological loop as a language learning device. , 1998, Psychological review.

[14]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[15]  John E. Desmond,et al.  Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task , 2005, Neuropsychologia.

[16]  C. Pallier,et al.  Left insula activation: a marker for language attainment in bilinguals. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Steve Majerus,et al.  Modulation of brain activity during phonological familiarization , 2005, Brain and Language.

[18]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[19]  Robert J Zatorre,et al.  Word and nonword repetition in bilingual subjects: A PET study , 2006, Human brain mapping.

[20]  Norihiro Sadato,et al.  Frontoparietal network involved in successful retrieval from episodic memory. Spatial and temporal analyses using fMRI and ERP. , 2006, Cerebral cortex.

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

[22]  Julie A Fiez,et al.  Functional dissociations within the inferior parietal cortex in verbal working memory , 2004, NeuroImage.

[23]  Edward F. Jackson,et al.  An event-related fMRI investigation of phonological versus semantic short-term memory , 2003, Journal of Neurolinguistics.

[24]  C. Marshuetz,et al.  Order information in working memory: an integrative review of evidence from brain and behavior. , 2005, Psychological bulletin.

[25]  A. Baddeley,et al.  When long-term learning depends on short-term storage , 1988 .

[26]  Marie Poirier,et al.  Immediate serial recall of words and nonwords: Tests of the retrieval-based hypothesis , 2000, Psychonomic bulletin & review.

[27]  B. MacWhinney,et al.  Vocabulary Acquisition and Verbal Short-Term Memory: Computational and Neural Bases , 1997, Brain and Language.

[28]  Steve Majerus,et al.  Verbal short-term memory and temporary activation of language representations: the importance of distinguishing item and order information , 2009 .

[29]  S E Petersen,et al.  A positron emission tomography study of the short-term maintenance of verbal information , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  S. Dehaene,et al.  Differential Contributions of the Left and Right Inferior Parietal Lobules to Number Processing , 1999, Journal of Cognitive Neuroscience.

[31]  Todd S Woodward,et al.  The influence of working memory load on phase specific patterns of cortical activity. , 2004, Brain research. Cognitive brain research.

[32]  N. Burgess,et al.  A revised model of short-term memory and long-term learning of verbal sequences , 2006 .

[33]  C. Frankish,et al.  Phonotactic influences on short-term memory. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[34]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[35]  Word frequency effects in immediate serial recall: Item familiarity and item co‐occurrence have the same effect , 2005, Memory.

[36]  R. Elliott,et al.  Differential Neural Responses during Performance of Matching and Nonmatching to Sample Tasks at Two Delay Intervals , 1999, The Journal of Neuroscience.

[37]  Ioulia Kovelman,et al.  Bilingual and monolingual brains compared: A functional magnetic resonance imaging investigation of syntactic processing and a possible “neural signature” of bilingualism , 2008 .

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

[39]  A. Baddeley,et al.  Phonological memory and vocabulary development during the early school years: A longitudinal study. , 1992 .

[40]  Steve Majerus,et al.  Exploring the relationship between new word learning and short-term memory for serial order recall, item recall, and item recognition , 2006 .

[41]  E. Service Phonology, Working Memory, and Foreign-language Learning , 1992, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[42]  Charles Hulme,et al.  Effects of word frequency and age of acquisition on short-term memory span , 1994, Memory & cognition.

[43]  Theodore P Trouard,et al.  fMRI variability and the localization of languages in the bilingual brain , 2003, Neuroreport.

[44]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[45]  Prahlad Gupta,et al.  Examining the Relationship between word Learning, Nonword Repetition, and Immediate Serial Recall in Adults , 2003, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[46]  John Jonides,et al.  Order Information in Working Memory: fMRI Evidence for Parietal and Prefrontal Mechanisms , 2000, Journal of Cognitive Neuroscience.

[47]  A. Baddeley,et al.  The Psychology of Learning and Motivation , 1974 .

[48]  Steve Majerus,et al.  Short-term memory and the left intraparietal sulcus: Focus of attention? Further evidence from a face short-term memory paradigm , 2007, NeuroImage.

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

[50]  Notger G. Müller,et al.  The functional neuroanatomy of visual conjunction search: a parametric fMRI study , 2003, NeuroImage.

[51]  Shigeru Sato,et al.  Cortical activation in the processing of passive sentences in L1 and L2: An fMRI study , 2006, NeuroImage.

[52]  Steven Laureys,et al.  Exploring the unity and diversity of the neural substrates of executive functioning , 2005, Human brain mapping.

[53]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[54]  Steve Majerus,et al.  The left intraparietal sulcus and verbal short-term memory: Focus of attention or serial order? , 2006, NeuroImage.

[55]  S Laureys,et al.  A PET investigation of lexicality and phonotactic frequency in oral language processing , 2002, Cognitive neuropsychology.

[56]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[57]  Alan C. Evans,et al.  Searching scale space for activation in PET images , 1996, Human brain mapping.

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

[59]  S. Gathercole,et al.  Contrasting contributions of phonological short‐term memory and long‐term knowledge to vocabulary learning in a foreign language , 2005, Memory.

[60]  Steve Majerus,et al.  Phonological short‐term memory networks following recovery from Landau and Kleffner syndrome , 2003, Human brain mapping.

[61]  Ioulia Kovelman,et al.  Bilingual and Monolingual Brains Compared: A Functional Magnetic Resonance Imaging Investigation of Syntactic Processing and a Possible Neural Signature of Bilingualism , 2008, Journal of Cognitive Neuroscience.

[62]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[63]  J. Fiez,et al.  A Comment on the Functional Localization of the Phonological Storage Subsystem of Working Memory , 1999, Brain and Cognition.

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

[65]  R. Frackowiak,et al.  Demonstrating the implicit processing of visually presented words and pseudowords. , 1996, Cerebral cortex.

[66]  W. Grodd,et al.  Articulatory/Phonetic Sequencing at the Level of the Anterior Perisylvian Cortex: A Functional Magnetic Resonance Imaging (fMRI) Study , 2000, Brain and Language.

[67]  C. Degueldre,et al.  Regional brain activity during working memory tasks. , 1996, Brain : a journal of neurology.

[68]  Eraldo Paulesu,et al.  The role of age of acquisition and language usage in early, high‐proficient bilinguals: An fMRI study during verbal fluency , 2003, Human brain mapping.

[69]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

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

[71]  Steve Majerus,et al.  Lexical learning in bilingual adults: The relative importance of short-term memory for serial order and phonological knowledge , 2008, Cognition.

[72]  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 .

[73]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[74]  Isabell Wartenburger,et al.  Early Setting of Grammatical Processing in the Bilingual Brain , 2003, Neuron.

[75]  S. Majerus,et al.  Contribution of lexico-semantic processes to verbal short-term memory tasks: A PET activation study , 2001, Memory.

[76]  Angela D. Friederici,et al.  Lateral Inferotemporal Cortex Maintains ConceptualSemantic Representations in Verbal Working Memory , 2007, Journal of Cognitive Neuroscience.

[77]  M. Page,et al.  Interactions Between Short-Term and Long-Term Memory in the Verbal Domain , 2008 .

[78]  Michael J. Spivey,et al.  Shared and separate systems in bilingual language processing: Converging evidence from eyetracking and brain imaging , 2003, Brain and Language.

[79]  N. Burgess Memory for Serial Order : A Network Model of the Phonological Loop and its Timing , 1999 .

[80]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI I. The Method , 2001, NeuroImage.