Neural bases of goal-directed implicit learning

Several neuropsychological and neuroimaging studies have been performed to clarify the neural bases of implicit learning, but the question of which brain regions are involved in different forms of implicit learning, including goal-directed learning and habit learning, has not yet been resolved. The present study sought to clarify the mechanisms of goal-directed implicit learning by examining the sugar production factory (SPF) task in conjunction with functional magnetic resonance imaging (fMRI). Several brain regions were identified that contribute to learning in the SPF task. Significant learning-related decreases in brain activity were found in the right inferior parietal lobule (IPL), left superior frontal gyrus, right medial frontal gyrus, cerebellar vermis, and left inferior frontal gyrus, while significant learning-related increases in activity were observed in the right inferior frontal gyrus, left precenteral gyrus and, left precuneus. Among these regions, we speculate that the IPL and medial frontal gyrus may specifically be involved in the early stage of goal-directed implicit learning. We also attempted to investigate the role of the striatum, which has a significant role in habit learning, during learning of the SPF task. The results of ROI analysis showed no learning-related change in the activity of the striatum. Although some of the observed learning-related activations in this study have also been previously reported in neuroimaging studies of habit learning, the possibility that specific brain regions involved in goal-direct implicit learning cannot be excluded.

[1]  Jan Noyes,et al.  Effect of experience and mode of presentation on problem solving , 2007, Comput. Hum. Behav..

[2]  Dianne C. Berry,et al.  The combination of explicit and implicit learning processes in task control , 1987 .

[3]  J. Desmond,et al.  The neural basis of visual skill learning: an fMRI study of mirror reading. , 1998, Cerebral cortex.

[4]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[5]  Nicole Wenderoth,et al.  Changes in Brain Activation during the Acquisition of a Multifrequency Bimanual Coordination Task: From the Cognitive Stage to Advanced Levels of Automaticity , 2005, The Journal of Neuroscience.

[6]  Carol A. Seger,et al.  Striatal activation during acquisition of a cognitive skill. , 1999, Neuropsychology.

[7]  P. A. Kolers The recognition of geometrically transformed text , 1968 .

[8]  Leslie G. Ungerleider,et al.  Experience-dependent changes in cerebellar contributions to motor sequence learning , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Hidenao Fukuyama,et al.  Activation of the precuneus is related to reduced reaction time in serial reaction time tasks , 2005, Neuroscience Research.

[10]  Marcia K. Johnson,et al.  FMRI evidence for an organization of prefrontal cortex by both type of process and type of information. , 2003, Cerebral cortex.

[11]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[12]  S. Killcross,et al.  Coordination of actions and habits in the medial prefrontal cortex of rats. , 2003, Cerebral cortex.

[13]  B. Balleine,et al.  Lesions of Medial Prefrontal Cortex Disrupt the Acquisition But Not the Expression of Goal-Directed Learning , 2005, The Journal of Neuroscience.

[14]  M. Gluck,et al.  Probabilistic classification learning in amnesia. , 1994, Learning & memory.

[15]  J.A. Anderson,et al.  Learning Motor Sequences with and without Knowledge of Governing Rules , 2005, Neurorehabilitation and neural repair.

[16]  A. Reber Implicit learning of artificial grammars , 1967 .

[17]  Dianne C. Berry,et al.  Implicit Learning , 1993 .

[18]  S. Dehaene,et al.  The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. , 2001, Cerebral cortex.

[19]  H. Eichenbaum,et al.  From Conditioning to Conscious Recollection , 2001 .

[20]  Martin P. Paulus,et al.  Superior temporal gyrus and insula provide response and outcome-dependent information during assessment and action selection in a decision-making situation , 2005, NeuroImage.

[21]  Michael P. Milham,et al.  Distinct neural mechanisms of risk and ambiguity: A meta-analysis of decision-making , 2006, NeuroImage.

[22]  D. LeBihan,et al.  Modulation of Parietal Activation by Semantic Distance in a Number Comparison Task , 2001, NeuroImage.

[23]  O. Hikosaka,et al.  Transition of Brain Activation from Frontal to Parietal Areas in Visuomotor Sequence Learning , 1998, The Journal of Neuroscience.

[24]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[25]  Peter McGeorge,et al.  The effects of concurrent verbalization on performance in a dynamic systems task , 1989 .

[26]  Leslie G. Ungerleider,et al.  Functional anatomy of motor skill learning. , 2002 .

[27]  Leslie G. Ungerleider,et al.  Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning , 2003, Neuropsychologia.

[28]  T. Robbins,et al.  Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates , 2004, Neuroscience & Biobehavioral Reviews.

[29]  B. Balleine,et al.  The role of prelimbic cortex in instrumental conditioning , 2003, Behavioural Brain Research.

[30]  L. Squire,et al.  The Neuropsychology of Memory , 1990 .

[31]  N. Cohen From Conditioning to Conscious Recollection Memory Systems of the Brain. Oxford Psychology Series, Volume 35. , 2001 .

[32]  D. Berry,et al.  Negative Correlations between Control Performance and Verbalizable Knowledge: Indicators for Implicit Learning in Process Control Tasks? , 1995, The Quarterly journal of experimental psychology. A, Human experimental psychology.

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

[34]  D. Broadbent,et al.  Interactive tasks and the implicit‐explicit distinction , 1988 .

[35]  Brian Butterworth,et al.  Are Subitizing and Counting Implemented as Separate or Functionally Overlapping Processes? , 2002, NeuroImage.

[36]  Stanislas Dehaene,et al.  Cerebral Pathways for Calculation: Double Dissociation between Rote Verbal and Quantitative Knowledge of Arithmetic , 1997, Cortex.

[37]  D. Broadbent,et al.  Two modes of learning for interactive tasks , 1988, Cognition.

[38]  R. Mathews,et al.  Insight without Awareness: On the Interaction of Verbalization, Instruction and Practice in a Simulated Process Control Task , 1989 .

[39]  C. Carter,et al.  Regional brain activation during concurrent implicit and explicit sequence learning. , 2004, Cerebral cortex.

[40]  B. Balleine,et al.  Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning , 2004, The European journal of neuroscience.

[41]  Axel Cleeremans,et al.  Implicit learning: news from the front , 1998, Trends in Cognitive Sciences.

[42]  E. Mayer,et al.  A pure case of Gerstmann syndrome with a subangular lesion. , 1999, Brain : a journal of neurology.

[43]  B. Balleine,et al.  Inactivation of dorsolateral striatum enhances sensitivity to changes in the action–outcome contingency in instrumental conditioning , 2006, Behavioural Brain Research.

[44]  Dianne C. Berry,et al.  The Role of Action in Implicit Learning , 1991 .

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

[46]  G. Deuschl,et al.  Patients with Parkinson's disease learn to control complex systems—an indication for intact implicit cognitive skill learning , 2006, Neuropsychologia.

[47]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[48]  Satrajit S. Ghosh,et al.  Region of interest based analysis of functional imaging data , 2003, NeuroImage.

[49]  B. Dubois,et al.  Functions of the left superior frontal gyrus in humans: a lesion study. , 2006, Brain : a journal of neurology.

[50]  D. Broadbent,et al.  On the Relationship between Task Performance and Associated Verbalizable Knowledge , 1984 .

[51]  Vivian V. Valentin,et al.  Determining the Neural Substrates of Goal-Directed Learning in the Human Brain , 2007, The Journal of Neuroscience.

[52]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.

[53]  B. Mazoyer,et al.  Neural Correlates of Simple and Complex Mental Calculation , 2001, NeuroImage.

[54]  Cyriel M. A. Pennartz,et al.  Learning-related changes in response patterns of prefrontal neurons during instrumental conditioning , 2003, Behavioural Brain Research.

[55]  S. Dehaene,et al.  Event-related fMRI analysis of the cerebral circuit for number comparison. , 1999, Neuroreport.

[56]  R. Poldrack,et al.  Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading. , 2001, Brain : a journal of neurology.

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

[58]  C Caltagirone,et al.  Implicit memory in parkinsonian patients: evidence for deficient skill learning. , 1996, European neurology.

[59]  Mauro PESENTI,et al.  Neuroanatomical substrates of Arabic number processing, numerical comparison and simple addition: A PET study. , 1998, NeuroImage.

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

[61]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[62]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[63]  M. Gluck,et al.  Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. , 2004, Brain : a journal of neurology.

[64]  P. Goldman-Rakic,et al.  Sustained Mnemonic Response in the Human Middle Frontal Gyrus during On-Line Storage of Spatial Memoranda , 2002, Journal of Cognitive Neuroscience.

[65]  David C. Plaut,et al.  A Connectionist Formulation of Learning in Dynamic Decision-Making Tasks , 1995 .

[66]  B. Postle,et al.  An fMRI Investigation of Cortical Contributions to Spatial and Nonspatial Visual Working Memory , 2000, NeuroImage.

[67]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[68]  J. Gabrieli Cognitive neuroscience of human memory. , 1998, Annual review of psychology.

[69]  C. I. Connolly,et al.  Building neural representations of habits. , 1999, Science.

[70]  L. Squire,et al.  Cognitive skill learning in amnesia , 1990, Psychobiology.

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

[72]  R. Masters,et al.  The role of working memory in motor learning and performance , 2003, Consciousness and Cognition.

[73]  Carol A. Seger,et al.  The Roles of the Caudate Nucleus in Human Classification Learning , 2005, The Journal of Neuroscience.

[74]  Daniel B. Willingham,et al.  Evidence for dissociable motor skills in Huntington’s disease patients , 1993, Psychobiology.

[75]  W. Schneider,et al.  Neuroimaging studies of practice-related change: fMRI and meta-analytic evidence of a domain-general control network for learning. , 2005, Brain research. Cognitive brain research.

[76]  D. Salmon,et al.  Neuropsychological evidence for multiple implicit memory systems: a comparison of Alzheimer's, Huntington's, and Parkinson's disease patients , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  M. Delazer,et al.  Arithmetic Facts without Meaning , 1997, Cortex.