Learning Arbitrary Visuomotor Associations: Temporal Dynamic of Brain Activity

Primates can give behavioral responses on the basis of arbitrary, context-dependent rules. When sensory instructions and behavioral responses are associated by arbitrary rules, these rules need to be learned. This study investigates the temporal dynamics of functional segregation at the basis of visuomotor associative learning in humans, isolating specific learning-related changes in neurovascular activity across the whole brain. We have used fMRI to measure human brain activity during performance of two tasks requiring the association of visual patterns with motor responses. Both tasks were learned by trial and error, either before (visuomotor control) or during (visuomotor learning) the scanning session. Epochs of tasks performance ( approximately 30 s) were alternated with a baseline period over the whole scanning session ( approximately 50 min). We have assessed both linear and nonlinear modulations in the differential signal between tasks, independently from overall task differences. The performance indices of the visuomotor learning task smoothly converged onto the values of a steady-state control condition, according to nonlinear timecourses. Specific visuomotor learning-related activity has been found over a distributed cortical network, centred on a temporo-prefrontal circuit. These cortical time-modulated activities were supported early in learning by the hippocampal/parahippocampal complex, and late in learning by the basal ganglia system. These findings suggest the inferior temporal and the ventral prefrontal cortex are critical neural nodes for integrating perceptual information with executive processes.

[1]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[2]  R. Passingham Premotor cortex: Sensory cues and movement , 1985, Behavioural Brain Research.

[3]  R. Passingham,et al.  Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis) , 1985, Behavioural Brain Research.

[4]  C. G. Phillips,et al.  A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis) , 1987, The Journal of comparative neurology.

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

[6]  A. Osman,et al.  Dimensional overlap: cognitive basis for stimulus-response compatibility--a model and taxonomy. , 1990, Psychological review.

[7]  S. Wise,et al.  Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  M. Taussig The Nervous System , 1991 .

[9]  E. Cabanis,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy and Mri , 1991 .

[10]  M. J. Eacott,et al.  Inferotemporal‐frontal Disconnection: The Uncinate Fascicle and Visual Associative Learning in Monkeys , 1992, The European journal of neuroscience.

[11]  R. Passingham The frontal lobes and voluntary action , 1993 .

[12]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[13]  P Alvarez,et al.  Memory consolidation and the medial temporal lobe: a simple network model. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[15]  D. Hoffman,et al.  Differential effects of muscimol microinjection into dorsal and ventral aspects of the premotor cortex of monkeys. , 1994, Journal of neurophysiology.

[16]  P. Goldman-Rakic,et al.  Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach Coordinate System. , 1995, Cerebral cortex.

[17]  A. Graybiel Building action repertoires: memory and learning functions of the basal ganglia , 1995, Current Opinion in Neurobiology.

[18]  M. Goodale,et al.  The visual brain in action , 1995 .

[19]  M Eimer,et al.  Stimulus-response compatibility and automatic response activation: evidence from psychophysiological studies. , 1995, Journal of experimental psychology. Human perception and performance.

[20]  S. Wise,et al.  Evolution of Directional Preferences in the Supplementary Eye Field during Acquisition of Conditional Oculomotor Associations , 1996, The Journal of Neuroscience.

[21]  Elisabeth A. Murray,et al.  Role of the hippocampus plus subjacent cortex but not amygdala in visuomotor conditional learning in rhesus monkeys. , 1996, Behavioral neuroscience.

[22]  M. Hallett,et al.  Frontal and parietal networks for conditional motor learning: a positron emission tomography study. , 1997, Journal of neurophysiology.

[23]  R. Passingham,et al.  Ventral Prefrontal Cortex Is Not Essential for Working Memory , 1997, The Journal of Neuroscience.

[24]  R. E. Passingham,et al.  Parietal cortex and movement I. Movement selection and reaching , 1997, Experimental Brain Research.

[25]  M. D’Esposito,et al.  The Inferential Impact of Global Signal Covariates in Functional Neuroimaging Analyses , 1998, NeuroImage.

[26]  J. Hollerman,et al.  Modifications of reward expectation-related neuronal activity during learning in primate striatum. , 1998, Journal of neurophysiology.

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

[28]  Anthony R. McIntosh,et al.  Task-Independent Effect of Time on rCBF , 1998, NeuroImage.

[29]  P. B. Cipolloni,et al.  Cortical connections of the frontoparietal opercular areas in the Rhesus monkey , 1999, The Journal of comparative neurology.

[30]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[31]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[32]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[33]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[34]  S. Wise,et al.  Role of the Hippocampal System in Conditional Motor Learning: Mapping Antecedents to Action , 1999, Hippocampus.

[35]  C R Genovese,et al.  Cortical networks subserving pursuit and saccadic eye movements in humans: An FMRI study , 1999, Human brain mapping.

[36]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[37]  R. Passingham,et al.  Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning , 2000, Experimental Brain Research.

[38]  M. Young,et al.  Computational analysis of functional connectivity between areas of primate cerebral cortex. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  S. Wise,et al.  Arbitrary associations between antecedents and actions , 2000, Trends in Neurosciences.

[40]  M Petrides,et al.  Orbitofrontal cortex: A key prefrontal region for encoding information. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  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..

[42]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

[43]  L. Squire,et al.  Contrasting Effects on Discrimination Learning after Hippocampal Lesions and Conjoint Hippocampal–Caudate Lesions in Monkeys , 2000, The Journal of Neuroscience.

[44]  R. E. Passingham,et al.  The cerebellum and cognition: cerebellar lesions impair sequence learning but not conditional visuomotor learning in monkeys , 2000, Neuropsychologia.

[45]  Ivan Toni,et al.  Contrasting the Dorsal and Ventral Visual Systems: Guidance of Movement versus Decision Making , 2001, NeuroImage.