An fMRI approach to particularize the frontoparietal network for visuomotor action monitoring: Detection of incongruence between test subjects’ actions and resulting perceptions

Contemporary theories of motor control assume that motor actions underlie a supervisory control system which utilizes reafferent sensory feedbacks of actions for comparison with the original motor programs. The functional network of visuomotor action monitoring is considered to include inferior parietal, lateral and medial prefrontal cortices. To study both sustained monitoring for visuomotor incongruence and the actual detection of incongruence, we used a hybrid fMRI epoch-/event-related design. The basic experimental task was a continuous motor task, comprising a simple racing game. Within certain blocks of this task, incongruence was artificially generated by intermittent takeover of control over the car by the computer. Fifteen male subjects were instructed to monitor for incongruence between their own and the observed actions in order to abstain from their own action whenever the computer took over control. As a result of both sustained monitoring and actual detection of visuomotor incongruence, the rostral inferior parietal lobule displayed a BOLD signal increase. In contrast, the prefrontal cortex (PFC) exhibited two different activation patterns. Dorsolateral (BA 9/46) and medial/cingulate (BA 8, BA 32) areas of the PFC displayed a greater increase of activation in sustained monitoring, while ventrolateral PFC showed greater event-related activation for the actual detection of visuomotor incongruence. Our results suggest that the rostral inferior parietal lobule is specifically involved in the reafferent comparison of the test subjects' own actions and visually perceived actions. Different activation patterns of the PFC may reflect different frontoparietal networks for sustained action monitoring and actual detection of reafferent incongruence.

[1]  J. Hirsch,et al.  A Neural Representation of Categorization Uncertainty in the Human Brain , 2006, Neuron.

[2]  D. Brooks,et al.  A PET study of voluntary movement in schizophrenic patients experiencing passivity phenomena (delusions of alien control). , 1997, Brain : a journal of neurology.

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

[4]  Mary A. Mayka,et al.  Intermittent visuomotor processing in the human cerebellum, parietal cortex, and premotor cortex. , 2006, Journal of neurophysiology.

[5]  T. Dietrich,et al.  Effects of Blood Estrogen Level on Cortical Activation Patterns during Cognitive Activation as Measured by Functional MRI , 2001, NeuroImage.

[6]  J. Marshall,et al.  The neural consequences of conflict between intention and the senses. , 1999, Brain : a journal of neurology.

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

[8]  W. Prinz Perception and Action Planning , 1997 .

[9]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[10]  M. Jeannerod,et al.  Defective recognition of one's own actions in patients with schizophrenia. , 2001, The American journal of psychiatry.

[11]  M. Jeannerod,et al.  Limited conscious monitoring of motor performance in normal subjects , 1998, Neuropsychologia.

[12]  L. Buxbaum,et al.  Reduced endogenous control in alien hand syndrome: evidence from naturalistic action , 2005, Neuropsychologia.

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

[14]  M. Jeannerod,et al.  Measuring time to awareness , 1991, Neuroreport.

[15]  Randy L. Buckner,et al.  Mixed blocked/event-related designs separate transient and sustained activity in fMRI , 2003, NeuroImage.

[16]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[17]  Kazuo Hiraki,et al.  The parietal role in the sense of self-ownership with temporal discrepancy between visual and proprioceptive feedbacks , 2005, NeuroImage.

[18]  J. Martí-Fàbregas,et al.  Alien Hand Sign after a Right Parietal Infarction , 2000, Cerebrovascular Diseases.

[19]  D. Yves von Cramon,et al.  Predicting events of varying probability: uncertainty investigated by fMRI , 2003, NeuroImage.

[20]  G. McCarthy,et al.  Decisions under Uncertainty: Probabilistic Context Influences Activation of Prefrontal and Parietal Cortices , 2005, The Journal of Neuroscience.

[21]  Gereon R Fink,et al.  Processing the spatial configuration of complex actions involves right posterior parietal cortex: An fMRI study with clinical implications , 2006, Human brain mapping.

[22]  Olaf B. Paulson,et al.  Similar brain networks for detecting visuo-motor and visuo-proprioceptive synchrony , 2006, NeuroImage.

[23]  Karl J. Friston,et al.  Comparing event-related and epoch analysis in blocked design fMRI , 2003, NeuroImage.

[24]  S. Blakemore,et al.  The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring , 2000, Psychological Medicine.

[25]  G. Goldberg,et al.  Medial frontal cortex infarction and the alien hand sign. , 1981, Archives of neurology.

[26]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[27]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[28]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[29]  C. Frith,et al.  A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory , 1996, Neuropsychologia.

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

[31]  N. Raz,et al.  Age, Sex and Regional Brain Volumes Predict Perceptual-Motor Skill Acquisition , 2005, Cortex.

[32]  D. Wolpert Computational approaches to motor control , 1997, Trends in Cognitive Sciences.

[33]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[34]  M. Goodale,et al.  An evolving view of duplex vision: separate but interacting cortical pathways for perception and action , 2004, Current Opinion in Neurobiology.

[35]  Stephen M. Rao,et al.  Neural Mechanisms of Visual Attention: Object-Based Selection of a Region in Space , 2000, Journal of Cognitive Neuroscience.

[36]  S. Yantis,et al.  Cortical mechanisms of feature-based attentional control. , 2003, Cerebral cortex.

[37]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  Leonardo Fogassi,et al.  Motor functions of the parietal lobe , 2005, Current Opinion in Neurobiology.

[39]  D. Wolpert,et al.  Abnormalities in the awareness and control of action. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  Hartwig R. Siebner,et al.  Linking Actions and Their Perceivable Consequences in the Human Brain , 2002, NeuroImage.

[41]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.