Anatomical Substrates of Visual and Auditory Miniature Second-language Learning

Longitudinal changes in brain activity during second language (L2) acquisition of a miniature finite-state grammar, named Wernickese, were identified with functional magnetic resonance imaging (fMRI). Participants learned either a visual sign language form or an auditory-verbal form to equivalent proficiency levels. Brain activity during sentence comprehension while hearing/viewing stimuli was assessed at low, medium, and high levels of proficiency in three separate fMRI sessions. Activation in the left inferior frontal gyrus (Broca's area) correlated positively with improving L2 proficiency, whereas activity in the right-hemisphere (RH) homologue was negatively correlated for both auditory and visual forms of the language. Activity in sequence learning areas including the premotor cortex and putamen also correlated with L2 proficiency. Modality-specific differences in the blood oxygenation level-dependent signal accompanying L2 acquisition were localized to the planum temporale (PT). Participants learning the auditory form exhibited decreasing reliance on bilateral PT sites across sessions. In the visual form, bilateral PT sites increased in activity between Session 1 and Session 2, then decreased in left PT activity from Session 2 to Session 3. Comparison of L2 laterality (as compared to L1 laterality) in auditory and visual groups failed to demonstrate greater RH lateralization for the visual versus auditory L2. These data establish a common role for Broca's area in language acquisition irrespective of the perceptual form of the language and suggest that L2s are processed similar to first languages even when learned after the critical period. The right frontal cortex was not preferentially recruited by visual language after accounting for phonetic/structural complexity and performance.

[1]  A. Braun,et al.  The neural organization of discourse: an H2 15O-PET study of narrative production in English and American sign language. , 2001, Brain : a journal of neurology.

[2]  A. Caramazza,et al.  Dissociation of algorithmic and heuristic processes in language comprehension: Evidence from aphasia , 1976, Brain and Language.

[3]  O. Hikosaka,et al.  Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. , 1996, Journal of neurophysiology.

[4]  M. Hallett,et al.  Complexity affects regional cerebral blood flow change during sequential finger movements , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  M. Chee,et al.  Mandarin and English Single Word Processing Studied with Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[6]  A. Friederici,et al.  Electrophysiological Evidence for Two Steps in Syntactic Analysis: Early Automatic and Late Controlled Processes , 1999, Journal of Cognitive Neuroscience.

[7]  Richard S. J. Frackowiak,et al.  Neural correlates of thinking in sign language , 1997, Neuroreport.

[8]  Yukihiko Fujii,et al.  Planum Temporale: Where Spoken and Written Language Meet , 2001, European Neurology.

[9]  Scott T. Grafton,et al.  Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. , 1997, Brain : a journal of neurology.

[10]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[11]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[12]  Richard A. Tennant,et al.  The American Sign Language Handshape Dictionary , 1998 .

[13]  Scott T. Grafton,et al.  Abstract and Effector-Specific Representations of Motor Sequences Identified with PET , 1998, The Journal of Neuroscience.

[14]  Arturo E. Hernandez,et al.  Language Switching and Language Representation in Spanish–English Bilinguals: An fMRI Study , 2000, NeuroImage.

[15]  M. Jung-Beeman Bilateral brain processes for comprehending natural language , 2005, Trends in Cognitive Sciences.

[16]  A. Friederici,et al.  Event-related brain potentials during natural speech processing: effects of semantic, morphological and syntactic violations. , 1993, Brain research. Cognitive brain research.

[17]  Ulrika Kahl,et al.  [The bilingual brain]. , 2002, Lakartidningen.

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

[19]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[20]  R. Passingham,et al.  The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study , 1998, NeuroImage.

[21]  J Pujol,et al.  [Functional MRI of the motor area]. , 1996, Neurologia.

[22]  A. Friederici,et al.  The brain basis of syntactic processes: functional imaging and lesion studies , 2003, NeuroImage.

[23]  S. Dehaene,et al.  Functional Neuroimaging of Speech Perception in Infants , 2002, Science.

[24]  M. Chee,et al.  Relative Language Proficiency Modulates BOLD Signal Change when Bilinguals Perform Semantic Judgments , 2001, NeuroImage.

[25]  Kuniyoshi L Sakai,et al.  Specialization in the Left Prefrontal Cortex for Sentence Comprehension , 2002, Neuron.

[26]  D Bavelier,et al.  Cerebral organization for language in deaf and hearing subjects: biological constraints and effects of experience. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  H. Freund,et al.  Premotor cortex and conditional motor learning in man. , 1990, Brain : a journal of neurology.

[28]  J P Rauschecker,et al.  Hemispheric specialization for English and ASL: left invariance‐right variability , 1998, Neuroreport.

[29]  D. Caplan,et al.  Processing of Visually Presented Sentences in Mandarin and English Studied with fMRI , 1999, Neuron.

[30]  T. Griffiths,et al.  The planum temporale as a computational hub , 2002, Trends in Neurosciences.

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

[32]  Scott T. Grafton,et al.  Functional Mapping of Sequence Learning in Normal Humans , 1995, Journal of Cognitive Neuroscience.

[33]  Ione Fine,et al.  Visual stimuli activate auditory cortex in the deaf , 2001, Nature Neuroscience.

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

[35]  Nobuko Kemmotsu,et al.  Functional MRI of motor sequence acquisition: effects of learning stage and performance. , 2002, Brain research. Cognitive brain research.

[36]  E. Zurif,et al.  The Critical Role of Group Studies in Neuropsychology: Comprehension Regularities in Broca's Aphasia , 1999, Brain and Language.

[37]  Scott T. Grafton,et al.  Neural Substrates of Response-based Sequence Learning using fMRI , 2004, Journal of Cognitive Neuroscience.

[38]  M. Gazzaniga,et al.  The new cognitive neurosciences , 2000 .

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

[40]  M. Garrett,et al.  Syntactically Based Sentence Processing Classes: Evidence from Event-Related Brain Potentials , 1991, Journal of Cognitive Neuroscience.

[41]  A. Friederici,et al.  Brain Correlates of Language Learning: The Neuronal Dissociation of Rule-Based versus Similarity-Based Learning , 2004, The Journal of Neuroscience.

[42]  Alan C. Evans,et al.  PET studies of phonetic processing of speech: review, replication, and reanalysis. , 1996, Cerebral cortex.

[43]  R. Kettner,et al.  Control of remembered reaching sequences in monkey , 1996, Experimental Brain Research.

[44]  Ralph-Axel Müller,et al.  Are nonlinguistic functions in “Broca’s area” prerequisites for language acquisition? FMRI findings from an ontogenetic viewpoint , 2004, Brain and Language.

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

[46]  J. A. Frost,et al.  Function of the left planum temporale in auditory and linguistic processing , 1996, NeuroImage.

[47]  G. Waters,et al.  PET Studies of Syntactic Processing with Auditory Sentence Presentation , 1999, NeuroImage.

[48]  Shinobu Masaki,et al.  Learning-induced neural plasticity associated with improved identification performance after training of a difficult second-language phonetic contrast , 2003, NeuroImage.

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

[50]  Alan C. Evans,et al.  Speech-like cerebral activity in profoundly deaf people processing signed languages: implications for the neural basis of human language. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[52]  C. Büchel,et al.  Broca's area and the language instinct , 2003, Nature Neuroscience.

[53]  R W Cox,et al.  Language processing is strongly left lateralized in both sexes. Evidence from functional MRI. , 1999, Brain : a journal of neurology.

[54]  Karl J. Friston,et al.  Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  Anne Cutler,et al.  Effects of sentential stress and word class upon comprehension in Broca's aphasics , 1980, Brain and Language.

[56]  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.

[58]  A J King,et al.  The development of topographically-aligned maps of visual and auditory space in the superior colliculus. , 1996, Progress in brain research.

[59]  Angela D. Friederici,et al.  Learning serial order of interval, spatial, and object information: An fMRI study on sequencing , 2001 .

[60]  Yasuki Noguchi,et al.  Selective Priming of Syntactic Processing by Event-Related Transcranial Magnetic Stimulation of Broca's Area , 2002, Neuron.

[61]  G. Waters,et al.  Activation of Broca's area by syntactic processing under conditions of concurrent articulation , 2000, Human brain mapping.

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

[63]  N. Alpert,et al.  Localization of Syntactic Comprehension by Positron Emission Tomography , 1996, Brain and Language.

[64]  A. Berthoz,et al.  Mental navigation along memorized routes activates the hippocampus, precuneus, and insula , 1997, Neuroreport.

[65]  D. V. von Cramon,et al.  Interval and ordinal properties of sequences are associated with distinct premotor areas. , 2001, Cerebral cortex.

[66]  Aaron J. Newman,et al.  A critical period for right hemisphere recruitment in American Sign Language processing , 2002, Nature Neuroscience.

[67]  Daniel J Driscoll,et al.  Sylvian fissure morphology in Prader-Willi syndrome and early-onset morbid obesity , 2007, Genetics in Medicine.

[68]  Marcel Adam Just,et al.  An fMRI Study of Bilingual Sentence Comprehension and Workload , 2002, NeuroImage.

[69]  Kuniyoshi L. Sakai,et al.  Sentence processing is uniquely human , 2003, Neuroscience Research.

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

[71]  F. Fazio,et al.  Brain processing of native and foreign languages , 1996, NeuroImage.

[72]  Ioulia Kovelman,et al.  Shining new light on the brain's “bilingual signature”: A functional Near Infrared Spectroscopy investigation of semantic processing , 2008, NeuroImage.

[73]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.