Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading.

The changes in brain activity related to skill learning and repetition priming in a mirror-reading task were examined using functional MRI. Subjects exhibited significant learning across five training sessions and this learning generalized significantly to different spatial transformations (inverted-mirror reversed text and normal letters spelled backwards). Mirror reading, compared with reading normal text, was associated with extensive activation in occipital, temporal, parietal and frontal regions. Learning to read mirror-reversed (MR) text was associated with increased activation in left inferior temporal, striatal, left inferior prefrontal and right cerebellar regions and with decreased activity in the left hippocampus and left cerebellum. Short-term repetition priming was associated with reduced activity in many of the regions active during mirror reading and extensive item-specific practice (long-term repetition priming) resulted in a virtual elimination of activity in those regions. Short- and long-term repetition priming thus appeared to rely upon common neural mechanisms. Nearly all of the regions exhibiting significant learning-related changes also exhibited increased repetition priming effects, suggesting common neural substrates for priming and skill learning in this task. Comparison of MR items with other spatially transformed typographies showed that the learning-related changes were general to all of the spatial transformations. The results confirm the importance of striatofrontal neural networks for the acquisition of skills, and suggest that skill learning and repetition priming may have common substrates within a particular task.

[1]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[2]  R. Nebes,et al.  Patterns of Hand Preference in a Student Population , 1975, Cortex.

[3]  Paul A. Kolers,et al.  Memorial Consequences of Automatized Encoding. , 1975 .

[4]  P. A. Kolers Reading a Year Later. , 1976 .

[5]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

[6]  J. Becker,et al.  Dissociations between skill learning and verbal recognition in amnesia and dementia. , 1984, Archives of neurology.

[7]  Keith D Horton,et al.  The role of semantic information in reading spatially transformed text , 1985, Cognitive Psychology.

[8]  Michael E. J. Masson,et al.  Identification of typographically transformed words: instance-based skill acquisition. , 1986 .

[9]  J. Saint-Cyr,et al.  Procedural learning and neostriatal dysfunction in man. , 1988, Brain : a journal of neurology.

[10]  H. Eichenbaum,et al.  Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. , 1988, Behavioral neuroscience.

[11]  D. Salmon,et al.  Impaired learning of a motor skill in patients with Huntington's disease. , 1988, Behavioral neuroscience.

[12]  Twila Tardif,et al.  Reading a week later: Perceptual and conceptual factors , 1989 .

[13]  M. Packard,et al.  Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  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.

[15]  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 .

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

[17]  S. Stone-Elander,et al.  Motor learning in man: a positron emission tomographic study. , 1990, Neuroreport.

[18]  G. Logan Repetition priming and automaticity: Common underlying mechanisms? , 1990, Cognitive Psychology.

[19]  Leslie G. Ungerleider,et al.  Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido‐nigral complex in the monkey , 1990, The Journal of comparative neurology.

[20]  D. Pandya,et al.  Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys , 1991, The Journal of comparative neurology.

[21]  S. Hashtroudi,et al.  Priming is independent of skill learning. , 1991, Journal of experimental psychology. Learning, memory, and cognition.

[22]  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.

[23]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[24]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[25]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

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

[27]  Mark G. Packard,et al.  Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat , 1994, Brain Research Bulletin.

[28]  R S Frackowiak,et al.  A PET study of cognitive strategies in normal subjects during language tasks. Influence of phonetic ambiguity and sequence processing on phoneme monitoring. , 1994, Brain : a journal of neurology.

[29]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[31]  K. D. Horton,et al.  Specificity of perceptual processing in rereading spatially transformed materials , 1995, Memory & cognition.

[32]  Karl J. Friston,et al.  Regional cerebral activity associated with the incidental processing of pseudo‐words , 1995 .

[33]  Jane S. Paulsen,et al.  Dissociations within nondeclarative memory in Huntington's disease. , 1996 .

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

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

[36]  D G Nishimura,et al.  Inhomogeneity correction using an estimated linear field map , 1996, Magnetic resonance in medicine.

[37]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[39]  J. B. Demb,et al.  Functional Magnetic Resonance Imaging of Semantic Memory Processes in the Frontal Lobes , 1996 .

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

[41]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[42]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[43]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

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

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

[46]  R A Poldrack,et al.  The relationship between skill learning and repetition priming: experimental and computational analyses. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[47]  K J Friston,et al.  The predictive value of changes in effective connectivity for human learning. , 1999, Science.

[48]  R. Poldrack Imaging Brain Plasticity: Conceptual and Methodological Issues— A Theoretical Review , 2000, NeuroImage.