Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex

This review article discusses mechanisms of how distinct behavioral operations are organized by different modules distributed in the frontal cortex. Cognitive manipulation often requires a flow of multiple elementary sub-operations processed in specialized brain regions. The dorsolateral prefrontal cortex (dlPFC) is likely responsible for attentional selection, which orients organisms' mental resources to behaviorally relevant information. The dorsal premotor cortex (PMd) is implicated to possess a functional gradient along the rostral-caudal axis. The rostral sector of the PMd (pre-PMd) is involved in various cognitive/premovement processes while its caudal sector (PMd proper) primarily controls actual movement. Neurophysiology studies in monkeys have shown that the pre-PMd, when functionally coupled with the dlPFC, may transform independent working memory items into a single sequence (sequence generation). A neuroimaging study has shown that the pre-PMd is indeed involved in sequence generation under the influence of the dlPFC in humans. It has been also indicated that the dlPFC and the pre-PMd are functionally coupled when attentional selection and sequence generation are to be unified for serial information processing. Functional interplay through the prefrontal-premotor connections may mediate the integration of specific sub-operations for multi-step cognitive manipulation. Furthermore, evidence from a meta-analysis of the imaging literature is argued for an idea that the coupling pattern with other frontal cortical areas may characterize of the function of the pre-PMd and PMd proper in various motor and cognitive tasks.

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

[2]  R. Passingham,et al.  The role of premotor and parietal cortex in the direction of action , 1982, Brain Research.

[3]  I. Toni,et al.  Integration of target and effector information in the human brain during reach planning. , 2007, Journal of neurophysiology.

[4]  M. Hallett,et al.  Brain activity during visuomotor behavior triggered by arbitrary and spatially constrained cues: an fMRI study in humans , 2006, Experimental Brain Research.

[5]  M. Banich,et al.  Functional dissociation of attentional selection within PFC: response and non-response related aspects of attentional selection as ascertained by fMRI. , 2006, Cerebral cortex.

[6]  S. Miyachi,et al.  Input–output organization of the rostral part of the dorsal premotor cortex, with special reference to its corticostriatal projection , 2004, Neuroscience Research.

[7]  M. Hallett,et al.  Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. , 2008, Cerebral cortex.

[8]  M. Honda,et al.  Modality-Specific Cognitive Function of Medial and Lateral Human Brodmann Area 6 , 2005, The Journal of Neuroscience.

[9]  G. Pagnoni,et al.  The neural correlates of the affective response to unreciprocated cooperation , 2008, Neuropsychologia.

[10]  Edward E. Smith,et al.  A parametric study of prefrontal cortex involvement in human working memory , 1996, NeuroImage.

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

[12]  J. Tanji,et al.  Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties , 2007, Current Opinion in Neurobiology.

[13]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

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

[15]  D. Boussaoud Attention versus Intention in the Primate Premotor Cortex , 2001, NeuroImage.

[16]  M. Petrides,et al.  Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[19]  C Galletti,et al.  Superior area 6 afferents from the superior parietal lobule in the macaque monkey , 1998, The Journal of comparative neurology.

[20]  M. Petrides Visuo-motor conditional associative learning after frontal and temporal lesions in the human brain , 1997, Neuropsychologia.

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

[22]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[23]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[24]  J. Tanji,et al.  Representation of the temporal order of visual objects in the primate lateral prefrontal cortex. , 2003, Journal of neurophysiology.

[25]  Takashi Hanakawa,et al.  Behavioral / Systems / Cognitive Functional Coupling of Human Prefrontal and Premotor Areas during Cognitive Manipulation , 2007 .

[26]  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.

[27]  M. Honda,et al.  The role of rostral Brodmann area 6 in mental-operation tasks: an integrative neuroimaging approach. , 2002, Cerebral cortex.

[28]  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..

[29]  N. Cohen,et al.  Prefrontal regions play a predominant role in imposing an attentional 'set': evidence from fMRI. , 2000, Brain research. Cognitive brain research.

[30]  J. Kaas,et al.  Movement representation in the dorsal and ventral premotor areas of owl monkeys: A microstimulation study , 1996, The Journal of comparative neurology.

[31]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[32]  Kenichi Ohki,et al.  Conversion of Working Memory to Motor Sequence in the Monkey Premotor Cortex , 2003, Science.

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

[34]  Michiyo Iba,et al.  Involvement of the dorsolateral prefrontal cortex of monkeys in visuospatial target selection. , 2003, Journal of neurophysiology.

[35]  Arthur F. Kramer,et al.  fMRI Studies of Stroop Tasks Reveal Unique Roles of Anterior and Posterior Brain Systems in Attentional Selection , 2000, Journal of Cognitive Neuroscience.

[36]  Rick Grush,et al.  The emulation theory of representation: Motor control, imagery, and perception , 2004, Behavioral and Brain Sciences.

[37]  O. Foerster,et al.  THE MOTOR CORTEX IN MAN IN THE LIGHT OF HUGHLINGS JACKSON'S DOCTRINES , 1936 .

[38]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Jun Tanji,et al.  Integration of target and body-part information in the premotor cortex when planning action , 2000, Nature.

[40]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[41]  Jun Tanji,et al.  Area-selective neuronal activity in the dorsolateral prefrontal cortex for information retrieval and action planning. , 2004, Journal of neurophysiology.

[42]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[43]  Paul B. Johnson,et al.  Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. , 1996, Cerebral cortex.

[44]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[45]  M. Petrides Motor conditional associative-learning after selective prefrontal lesions in the monkey , 1982, Behavioural Brain Research.

[46]  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.

[47]  H. Freund,et al.  Lesions of premotor cortex in man. , 1985, Brain : a journal of neurology.

[48]  D. Boussaoud,et al.  Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. , 2002, Journal of neurophysiology.

[49]  Scott T. Grafton,et al.  Graspable objects grab attention when the potential for action is recognized , 2003, Nature Neuroscience.

[50]  L. Cohen,et al.  Reorganization of the human ipsilesional premotor cortex after stroke. , 2004, Brain : a journal of neurology.

[51]  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.

[52]  Michael Petrides,et al.  Local Morphology Predicts Functional Organization of the Dorsal Premotor Region in the Human Brain , 2006, The Journal of Neuroscience.

[53]  M. Hallett,et al.  Amodal imagery in rostral premotor areas , 2004, Behavioral and Brain Sciences.

[54]  E. Hoshi Functional specialization within the dorsolateral prefrontal cortex: A review of anatomical and physiological studies of non-human primates , 2006, Neuroscience Research.

[55]  Vittorio Gallese,et al.  Somatotopic organization of the lateral part of area F2 (dorsal premotor cortex) of the macaque monkey. , 2003, Journal of neurophysiology.

[56]  Takashi Hanakawa,et al.  Differential activity in the premotor cortex subdivisions in humans during mental calculation and verbal rehearsal tasks: a functional magnetic resonance imaging study , 2003, Neuroscience Letters.

[57]  M. Denis,et al.  Functional Anatomy of Spatial Mental Imagery Generated from Verbal Instructions , 1996, The Journal of Neuroscience.

[58]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[59]  M. Petrides Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man , 1985, Neuropsychologia.

[60]  E. Miller,et al.  The Prefrontal Cortex Complex Neural Properties for Complex Behavior , 1999, Neuron.

[61]  Bruce R. Rosen,et al.  Activity in Ventrolateral and Mid-Dorsolateral Prefrontal Cortex during Nonspatial Visual Working Memory Processing: Evidence from Functional Magnetic Resonance Imaging , 2000, NeuroImage.

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

[63]  E. Miller,et al.  THE PREFRONTAL CORTEX AND COGNITIVE CONTROL , 2000 .

[64]  M. Petrides,et al.  Specialized systems for the processing of mnemonic information within the primate frontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[65]  James B. Rowe,et al.  Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory , 2001, NeuroImage.

[66]  K Friston,et al.  Signal-, set- and movement-related activity in the human brain: an event-related fMRI study. , 1999, Cerebral cortex.

[67]  M. Petrides The effect of periarcuate lesions in the monkey on the performance of symmetrically and asymmetrically reinforced visual and auditory go, no- go tasks , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  N. P. Bichot,et al.  Converging evidence from microstimulation, architecture, and connections for multiple motor areas in the frontal and cingulate cortex of prosimian primates , 2000, The Journal of comparative neurology.

[69]  M. Mesulam,et al.  Cortical afferent input to the principals region of the rhesus monkey , 1985, Neuroscience.

[70]  R. McLean,et al.  Effects of induced chunking on temporal aspects of serial recitation. , 1967, Journal of experimental psychology.

[71]  J. Tanji,et al.  Functional specialization in dorsal and ventral premotor areas. , 2004, Progress in brain research.

[72]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[73]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[74]  G E Alexander,et al.  Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. , 1997, Journal of neurophysiology.

[75]  R. Coppola,et al.  Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. , 1999, Cerebral cortex.

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

[77]  R. Knight,et al.  The functional neuroanatomy of working memory: Contributions of human brain lesion studies , 2006, Neuroscience.

[78]  G. Luppino,et al.  ß Federation of European Neuroscience Societies Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey , 2022 .

[79]  J. Binder,et al.  Functional MRI evidence for subcortical participation in conceptual reasoning skills , 1997, Neuroreport.

[80]  John F. Kalaska,et al.  Neural correlates of mental rehearsal in dorsal premotor cortex , 2004, Nature.

[81]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[82]  S. Wise,et al.  The premotor cortex of the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[83]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations , 2007, The Journal of Neuroscience.

[84]  M. Hallett,et al.  Functional properties of brain areas associated with motor execution and imagery. , 2003, Journal of neurophysiology.

[85]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[86]  Takashi Hanakawa,et al.  Neural correlates underlying mental calculation in abacus experts: a functional magnetic resonance imaging study , 2003, NeuroImage.