A neuroanatomically grounded Hebbian-learning model of attention–language interactions in the human brain

Meaningful familiar stimuli and senseless unknown materials lead to different patterns of brain activation. A late major neurophysiological response indexing ‘sense’ is the negative component of event‐related potential peaking at around 400 ms (N400), an event‐related potential that emerges in attention‐demanding tasks and is larger for senseless materials (e.g. meaningless pseudowords) than for matched meaningful stimuli (words). However, the mismatch negativity (latency 100–250 ms), an early automatic brain response elicited under distraction, is larger to words than to pseudowords, thus exhibiting the opposite pattern to that seen for the N400. So far, no theoretical account has been able to reconcile and explain these findings by means of a single, mechanistic neural model. We implemented a neuroanatomically grounded neural network model of the left perisylvian language cortex and simulated: (i) brain processes of early language acquisition and (ii) cortical responses to familiar word and senseless pseudoword stimuli. We found that variation of the area‐specific inhibition (the model correlate of attention) modulated the simulated brain response to words and pseudowords, producing either an N400‐ or a mismatch negativity‐like response depending on the amount of inhibition (i.e. available attentional resources). Our model: (i) provides a unifying explanatory account, at cortical level, of experimental observations that, so far, had not been given a coherent interpretation within a single framework; (ii) demonstrates the viability of purely Hebbian, associative learning in a multilayered neural network architecture; and (iii) makes clear predictions on the effects of attention on latency and magnitude of event‐related potentials to lexical items. Such predictions have been confirmed by recent experimental evidence.

[1]  Philipp Slusallek,et al.  Introduction to real-time ray tracing , 2005, SIGGRAPH Courses.

[2]  Christina M. Krause,et al.  Early and Late Mismatch Negativity Elicited by Words and Speech-Like Stimuli in Children , 2001, Brain and Language.

[3]  F. Pulvermüller,et al.  Language outside the focus of attention: The mismatch negativity as a tool for studying higher cognitive processes , 2006, Progress in Neurobiology.

[4]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[5]  Gèunther Palm,et al.  Neural Assemblies: An Alternative Approach to Artificial Intelligence , 1982 .

[6]  J. Eggert,et al.  Unifying framework for neuronal assembly dynamics. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[7]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[8]  F. T. Husain,et al.  Relating neuronal dynamics for auditory object processing to neuroimaging activity: a computational modeling and an fMRI study , 2004, NeuroImage.

[9]  Matthew A. Lambon Ralph,et al.  Lateralization of ventral and dorsal auditory-language pathways in the human brain , 2005, NeuroImage.

[10]  Günther Palm,et al.  An Associative Cortical Model of Language Understanding and Action Planning , 2005, IWINAC.

[11]  T. Paus,et al.  Seeing and hearing speech excites the motor system involved in speech production , 2003, Neuropsychologia.

[12]  G. Marchetti Commentary on Friedemann Pulvermüller's The Neuroscience of Language. On Brain Circuits of Words and Serial Order , 2007 .

[13]  R. Traub,et al.  Neuronal networks for induced ‘40 Hz’ rhythms , 1996, Trends in Neurosciences.

[14]  Leila Reddy,et al.  Coding of visual objects in the ventral stream , 2006, Current Opinion in Neurobiology.

[15]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[16]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[17]  J. Cowan,et al.  A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue , 1973, Kybernetik.

[18]  M. Kutas,et al.  Semantic processing and memory for attended and unattended words in dichotic listening: behavioral and electrophysiological evidence. , 1995, Journal of experimental psychology. Human perception and performance.

[19]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[20]  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 .

[21]  T. Sejnowski,et al.  Storing covariance with nonlinearly interacting neurons , 1977, Journal of mathematical biology.

[22]  Gustavo Deco,et al.  Computational neuroscience of vision , 2002 .

[23]  R. Näätänen,et al.  Early selective-attention effect on evoked potential reinterpreted. , 1978, Acta psychologica.

[24]  J. Wickens A Theory of the Striatum , 1993 .

[25]  Stefan Wermter,et al.  Grounding Neural Robot Language in Action , 2005, Biomimetic Neural Learning for Intelligent Robots.

[26]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[27]  P. Nunez The brain wave equation: a model for the EEG , 1974 .

[28]  W. Freeman Models of the dynamics of neural populations. , 1978, Electroencephalography and clinical neurophysiology. Supplement.

[29]  Stefan Wermter,et al.  Learning robot actions based on self-organising language memory , 2003, Neural Networks.

[30]  Günther Palm,et al.  Biomimetic Neural Learning for Intelligent Robots - Intelligent Systems, Cognitive Robotics, and Neuroscience , 2005, Biomimetic Neural Learning for Intelligent Robots.

[31]  D. Zipser,et al.  A spiking network model of short-term active memory , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Stefan Wermter,et al.  Towards multimodal neural robot learning , 2004, Robotics Auton. Syst..

[33]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.

[34]  F. Pulvermüller The Neuroscience of Language , 2003 .

[35]  O. L. Z. Book Review: The Organization of Behaviour: A Neuropsychological Theory , 1950 .

[36]  G. Westermann,et al.  A new model of sensorimotor coupling in the development of speech , 2004, Brain and Language.

[37]  A. Cowey,et al.  Vertical organization of neurones accumulating 3H-GABA in visual cortex of rhesus monkey , 1981, Nature.

[38]  Friedemann Pulvermüller,et al.  The Neuroscience of Language: On Brain Circuits of Words and Serial Order , 2003 .

[39]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[40]  Mingqi Deng,et al.  Winner-take-all networks , 1992 .

[41]  Michael C. Doyle,et al.  Modulation of event-related potentials by word repetition: the role of visual selective attention. , 1993, Psychophysiology.

[42]  J. Duncan Attention, intelligence, and the frontal lobes. , 1995 .

[43]  G S Dell,et al.  A spreading-activation theory of retrieval in sentence production. , 1986, Psychological review.

[44]  E. Yeterian,et al.  MRI-Based Topographic Parcellation of Human Cerebral White Matter and Nuclei II. Rationale and Applications with Systematics of Cerebral Connectivity , 1999, NeuroImage.

[45]  Nick Chater,et al.  Connectionist natural language processing: the state of the art , 1999, Cogn. Sci..

[46]  S. Schultz Principles of Neural Science, 4th ed. , 2001 .

[47]  Friedemann Pulvermüller,et al.  Neurophysiological evidence of memory traces for words in the human brain , 2002, Neuroreport.

[48]  H. C. LONGUET-HIGGINS,et al.  Non-Holographic Associative Memory , 1969, Nature.

[49]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[50]  T. Powell,et al.  The basic uniformity in structure of the neocortex. , 1980, Brain : a journal of neurology.

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

[52]  W. Singer,et al.  Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation , 1993, Trends in Neurosciences.

[53]  N. Moray Attention in Dichotic Listening: Affective Cues and the Influence of Instructions , 1959 .

[54]  Günther Palm,et al.  Associative memory and threshold control in neural networks , 1987 .

[55]  Mark S. Seidenberg,et al.  Impairments in verb morphology after brain injury: a connectionist model. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[56]  A. Agmon,et al.  Vertical bias in dendritic trees of non-pyramidal neocortical neurons expressing GAD67-GFP in vitro. , 2001, Cerebral cortex.

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

[58]  G. Deco,et al.  Cooperation and biased competition model can explain attentional filtering in the prefrontal cortex , 2004, The European journal of neuroscience.

[59]  E. Rolls,et al.  What and Where in Visual Working Memory: A Computational Neurodynamical Perspective for Integrating fMRI and Single-Neuron Data , 2004, Journal of Cognitive Neuroscience.

[60]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[61]  Paavo Alku,et al.  Memory Traces for Words as Revealed by the Mismatch Negativity , 2001, NeuroImage.

[62]  K. Alho,et al.  Intermodal selective attention. I. Effects on event-related potentials to lateralized auditory and visual stimuli. , 1992, Electroencephalography and clinical neurophysiology.

[63]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[64]  M. Kutas,et al.  Reading senseless sentences: brain potentials reflect semantic incongruity. , 1980, Science.

[65]  William D. Marslen-Wilson,et al.  The time course of visual word recognition as revealed by linear regression analysis of ERP data , 2006, NeuroImage.

[66]  E. Rolls,et al.  Attention, short-term memory, and action selection: A unifying theory , 2005, Progress in Neurobiology.

[67]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[68]  Michael A. Arbib,et al.  The handbook of brain theory and neural networks , 1995, A Bradford book.

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

[70]  Eduardo Miranda,et al.  Modelling the Development of Mirror Neurons for Auditory-Motor Integration , 2002 .

[71]  G Pfurtscheller,et al.  Computational model of thalamo-cortical networks: dynamical control of alpha rhythms in relation to focal attention. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[72]  Friedemann Pulverm Uuml,et al.  Words in the brain's language , 1999 .

[73]  J. Duncan The locus of interference in the perception of simultaneous stimuli. , 1980, Psychological review.

[74]  J. Duncan,et al.  Visual search and stimulus similarity. , 1989, Psychological review.

[75]  James L. McClelland,et al.  Understanding normal and impaired word reading: computational principles in quasi-regular domains. , 1996, Psychological review.

[76]  Paavo Alku,et al.  Automatic Auditory Processing of English Words as Indexed by the Mismatch Negativity, Using a Multiple Deviant Paradigm , 2004, Ear and hearing.

[77]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[78]  Friedemann Pulvermüller,et al.  Brain mechanisms linking language and action , 2005, Nature Reviews Neuroscience.

[79]  Gary S. Dell,et al.  Connectionist models of language production: lexical access and grammatical encoding , 1999, Cogn. Sci..

[80]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[81]  J. Duncan EPS Mid-Career Award 2004: Brain mechanisms of attention , 2006, Quarterly journal of experimental psychology.

[82]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[83]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[84]  M. Iacoboni,et al.  Listening to speech activates motor areas involved in speech production , 2004, Nature Neuroscience.

[85]  William H. Press,et al.  Numerical recipes in C (2nd ed.): the art of scientific computing , 1992 .

[86]  R. C. Tees Review of The organization of behavior: A neuropsychological theory. , 2003 .

[87]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[88]  N. Drasdo Eye, brain, and vision David H. Hubel Scientific American Library Book — distributed by W. H. Freeman, New York, £15.95 , 1990 .

[89]  Freeman Wj Models of the dynamics of neural populations. , 1978 .

[90]  W. Press,et al.  Numerical Recipes in C++: The Art of Scientific Computing (2nd edn)1 Numerical Recipes Example Book (C++) (2nd edn)2 Numerical Recipes Multi-Language Code CD ROM with LINUX or UNIX Single-Screen License Revised Version3 , 2003 .

[91]  Roland Heim,et al.  Theoretical Approaches to Complex Systems , 1978 .

[92]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[93]  G. Holmes The prefrontal cortex: Anatomy, physiology, and neuropsychology of the frontal lobe (2nd ed.) , 1989 .

[94]  Fabrice Wendling,et al.  Relevance of nonlinear lumped-parameter models in the analysis of depth-EEG epileptic signals , 2000, Biological Cybernetics.

[95]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[96]  F. Pulvermüller Brain reflections of words and their meaning , 2001, Trends in Cognitive Sciences.

[97]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[98]  K. Jellinger Cortex and Mind. Unifying Cognition , 2003 .

[99]  Friedemann Pulvermüller,et al.  Constituents of a neurological theory of language , 1992 .

[100]  Satrajit S. Ghosh,et al.  Neural modeling and imaging of the cortical interactions underlying syllable production , 2006, Brain and Language.

[101]  Friedemann Pulvermüller,et al.  Sequence Detector Networks and Associative Learning of Grammatical Categories , 2005, Biomimetic Neural Learning for Intelligent Robots.

[102]  James L. McClelland,et al.  A distributed model of human learning and memory , 1986 .

[103]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[104]  Charles F. Stevens,et al.  How Cortical Interconnectedness Varies with Network Size , 1989, Neural Computation.

[105]  Karl J. Friston,et al.  A neural mass model for MEG/EEG: coupling and neuronal dynamics , 2003, NeuroImage.

[106]  David C. Plaut,et al.  Are non-semantic morphological effects incompatible with a distributed connectionist approach to lexical processing? , 2000 .

[107]  R. O’Reilly Six principles for biologically based computational models of cortical cognition , 1998, Trends in Cognitive Sciences.

[108]  William Bialek,et al.  Adaptive Rescaling Maximizes Information Transmission , 2000, Neuron.

[109]  Alon Sinai,et al.  Electrophysiological Evidence for Priming in Response to Words and Pseudowords in First and Second Language , 2002, Brain and Language.

[110]  Ad Aertsen,et al.  Editorial: Cell Assemblies , 2003 .

[111]  E. Yund,et al.  Phonemes, intensity and attention: differential effects on the mismatch negativity (MMN). , 1999, The Journal of the Acoustical Society of America.

[112]  J. Duncan Cooperating brain systems in selective perception and action. , 1996 .

[113]  James L. McClelland,et al.  A distributed, developmental model of word recognition and naming. , 1989, Psychological review.

[114]  Günther Palm,et al.  Scene segmentation by spike synchronization in reciprocally connected visual areas. I. Local effects of cortical feedback , 2002, Biological Cybernetics.

[115]  D. Norris Shortlist: a connectionist model of continuous speech recognition , 1994, Cognition.

[116]  J. Buhle,et al.  Typologies of attentional networks , 2006, Nature Reviews Neuroscience.

[117]  P. Milner,et al.  Neural Representations: Some Old Problems Revisited , 1996, Journal of Cognitive Neuroscience.

[118]  Risto Miikkulainen,et al.  Computational Maps in the Visual Cortex , 2005 .

[119]  Marta Kutas,et al.  Interplay between computational models and cognitive electrophysiology in visual word recognition , 2007, Brain Research Reviews.

[120]  N. Cowan,et al.  The cocktail party phenomenon revisited: attention and memory in the classic selective listening procedure of Cherry (1953). , 1995, Journal of experimental psychology. General.

[121]  William D. Marslen-Wilson,et al.  A Connectionist Model of Phonological Representation in Speech Perception , 1995, Cogn. Sci..

[122]  F. Bloom,et al.  Magnetoencephalographic recordings demonstrate attentional modulation of mismatch-related neural activity in human auditory cortex. , 1998, Psychophysiology.

[123]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[124]  Morten H. Christiansen,et al.  Connectionist psycholinguistics: capturing the empirical data , 2001, Trends in Cognitive Sciences.

[125]  M. Young,et al.  The architecture of visual cortex and inferential processes in vision. , 2000, Spatial vision.

[126]  T. Paus,et al.  Modulation of Motor Excitability during Speech Perception: The Role of Broca's Area , 2004, Journal of Cognitive Neuroscience.

[127]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[128]  N. Cowan,et al.  The cocktail party phenomenon revisited: how frequent are attention shifts to one's name in an irrelevant auditory channel? , 1995, Journal of experimental psychology. Learning, memory, and cognition.

[129]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[130]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[131]  B. Horwitz,et al.  Integrating electrophysiological and anatomical experimental data to create a large-scale model that simulates a delayed match-to-sample human brain imaging study. , 1998, Cerebral cortex.

[132]  D. Hubel Eye, brain, and vision , 1988 .

[133]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[134]  R. Näätänen,et al.  Intermodal selective attention. II. Effects of attentional load on processing of auditory and visual stimuli in central space. , 1992, Electroencephalography and clinical neurophysiology.

[135]  Gustavo Deco,et al.  Large-scale neural model for visual attention: integration of experimental single-cell and fMRI data. , 2002, Cerebral cortex.

[136]  Valentino Braitenberg,et al.  Brain Size and Number of Neurons: An Exercise in Synthetic Neuroanatomy , 2004, Journal of Computational Neuroscience.

[137]  L. Garey Cortex: Statistics and Geometry of Neuronal Connectivity, 2nd edn. By V. BRAITENBERG and A. SCHÜZ. (Pp. xiii+249; 90 figures; ISBN 3 540 63816 4). Berlin: Springer. 1998. , 1999 .

[138]  G. Rizzolatti,et al.  Speech listening specifically modulates the excitability of tongue muscles: a TMS study , 2002, The European journal of neuroscience.

[139]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[140]  F. Crépel,et al.  Homo‐ and heterosynaptic changes in efficacy are expressed in prefrontal neurons: An in vitro study in the rat , 1992, Synapse.

[141]  Friedemann Pulvermüller,et al.  A neuronal model of the language cortex , 2007, Neurocomputing.

[142]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.