Serial Organization of Human Behavior in the Inferior Parietal Cortex

The parietal cortex is involved in a wide range of cognitive functions in humans including associative functions between multiple sensorimotor spaces, attentional control, and working memory. Little is known, however, about the role and the functional organization of the parietal cortex in action planning and sequential cognition. Moreover, the respective contributions of parietal and frontal regions to action planning remains poorly understood. To address this issue, we designed a functional magnetic resonance imaging protocol requiring subjects to perform overlearned sequences of motor acts and sequences of cognitive tasks. The results reveal only a single bilateral region in the cerebral cortex located in the intraparietal sulcus (IPS; Brodmann's area 40) exhibiting sustained activations during the execution of both motor and task sequences. Additional analyses of phasic activations during sequence execution further suggest a functional dissociation between the left IPS, involved in representing and processing the abstract serial structure of ongoing behavioral sequences regardless of their hierarchical structure, and the right IPS, involved in preparing successive sensorimotor sets that compose such behavioral sequences. We show that this parietal system functionally differs from the frontal system that was previously identified as controlling action selection with respect to the hierarchical rather than serial structure of behavioral plans. Thus, our results reveal the central role of the bilateral intraparietal sulcus in high-order sequential cognition and suggest a major functional segregation within the frontoparietal network mediating action planning, with the frontal and parietal sector involved in processing the hierarchical and serial structure of action plans, respectively.

[1]  J. Fuster Prefrontal Cortex , 2018 .

[2]  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 .

[3]  Jun Tanji,et al.  Role for supplementary motor area cells in planning several movements ahead , 1994, Nature.

[4]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

[5]  M. Hallett,et al.  Complexity affects regional cerebral blood flow change during sequential finger movements , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  R. Dolan,et al.  Neural systems engaged by planning: a PET study of the Tower of London task , 1996, Neuropsychologia.

[7]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[8]  R. Passingham,et al.  The left parietal cortex and motor attention , 1997, Neuropsychologia.

[9]  F. Aboitiz,et al.  The evolutionary origin of the language areas in the human brain. A neuroanatomical perspective , 1997, Brain Research Reviews.

[10]  M. Hallett,et al.  The functional neuroanatomy of simple and complex sequential finger movements: a PET study. , 1998, Brain : a journal of neurology.

[11]  Scott T. Grafton,et al.  Abstract and Effector-Specific Representations of Motor Sequences Identified with PET , 1998, The Journal of Neuroscience.

[12]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[13]  M. Corbetta,et al.  Erratum to “Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines” , 2000, Nature Neuroscience.

[14]  Lars Nyberg,et al.  Age-Related Differences in Neural Activity during Item and Temporal-Order Memory Retrieval: A Positron Emission Tomography Study , 2000, Journal of Cognitive Neuroscience.

[15]  Fumitaka Homae,et al.  Sentence processing in the cerebral cortex , 2001, Neuroscience Research.

[16]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[17]  G. Leichnetz Connections of the medial posterior parietal cortex (area 7m) in the monkey , 2001, The Anatomical record.

[18]  Yale E. Cohen,et al.  A common reference frame for movement plans in the posterior parietal cortex , 2002, Nature Reviews Neuroscience.

[19]  Katsuyuki Sakai,et al.  Learning of sequences of finger movements and timing: frontal lobe and action-oriented representation. , 2002, Journal of neurophysiology.

[20]  E. Koechlin,et al.  Medial Prefrontal and Subcortical Mechanisms Underlying the Acquisition of Motor and Cognitive Action Sequences in Humans , 2002, Neuron.

[21]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[22]  John R Anderson,et al.  Neural mechanisms of planning: A computational analysis using event-related fMRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Shabtai Barash,et al.  Paradoxical activities: insight into the relationship of parietal and prefrontal cortices , 2003, Trends in Neurosciences.

[24]  J. Duncan,et al.  Encoding Strategies Dissociate Prefrontal Activity from Working Memory Demand , 2003, Neuron.

[25]  M. Rushworth,et al.  The left parietal and premotor cortices: motor attention and selection , 2003, NeuroImage.

[26]  M. Hallett,et al.  How self-initiated memorized movements become automatic: a functional MRI study. , 2004, Journal of neurophysiology.

[27]  S. Bunge How we use rules to select actions: A review of evidence from cognitive neuroscience , 2004, Cognitive, affective & behavioral neuroscience.

[28]  M. Brass,et al.  Decomposing Components of Task Preparation with Functional Magnetic Resonance Imaging , 2004, Journal of Cognitive Neuroscience.

[29]  Hans Forssberg,et al.  Dissociating brain regions controlling the temporal and ordinal structure of learned movement sequences , 2004, The European journal of neuroscience.

[30]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[31]  Marcel Brass,et al.  Selection for Cognitive Control: A Functional Magnetic Resonance Imaging Study on the Selection of Task-Relevant Information , 2004, The Journal of Neuroscience.

[32]  Koji Jimura,et al.  Multiple components of lateral posterior parietal activation associated with cognitive set shifting , 2005, NeuroImage.

[33]  A. Luxen,et al.  Involvement of both prefrontal and inferior parietal cortex in dual-task performance. , 2005, Brain research. Cognitive brain research.

[34]  Thomas R. Knösche,et al.  Who Comes First? The Role of the Prefrontal and Parietal Cortex in Cognitive Control , 2005, Journal of Cognitive Neuroscience.

[35]  Hans Forssberg,et al.  Effector‐independent voluntary timing: behavioural and neuroimaging evidence , 2005, The European journal of neuroscience.

[36]  Aysenil Belger,et al.  Dissociation of neural systems mediating shifts in behavioral response and cognitive set , 2005, NeuroImage.

[37]  E. Koechlin,et al.  Broca's Area and the Hierarchical Organization of Human Behavior , 2006, Neuron.

[38]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.