Effects of dorsolateral prefrontal cortex lesion on motor habit and performance assessed with manual grasping and control of force in macaque monkeys

In the context of an autologous adult neural cell ecosystem (ANCE) transplantation study, four intact adult female macaque monkeys underwent a unilateral biopsy of the dorsolateral prefrontal cortex (dlPFC) to provide the cellular material needed to obtain the ANCE. Monkeys were previously trained to perform quantitative motor (manual dexterity) tasks, namely, the “modified-Brinkman board” task and the “reach and grasp drawer” task. The aim of the present study was to extend preliminary data on the role of the prefrontal cortex in motor habit and test the hypothesis that dlPFC contributes to predict the grip force required when a precise level of force to be generated is known beforehand. As expected for a small dlPFC biopsy, neither the motor performance (score) nor the spatiotemporal motor sequences were affected in the “modified-Brinkman board” task, whereas significant changes (mainly decreases) in the maximal grip force (force applied on the drawer knob) were observed in the “reach and grasp drawer” task. The present data in the macaque monkey related to the prediction of grip force are well in line with the previous fMRI data reported for human subjects. Moreover, the ANCE transplantation strategy (in the case of stroke or Parkinson’s disease) based on biopsy in dlPFC does not generate unwanted motor consequences, at least as far as motor habit and motor performance are concerned in the context of a sequential grasping a small objects, which does not require the development of significant force levels.

[1]  U. Halsband,et al.  Motor learning in man: A review of functional and clinical studies , 2006, Journal of Physiology-Paris.

[2]  P. Goldman-Rakic Motor control function of the prefrontal cortex. , 1987, Ciba Foundation symposium.

[3]  J. Bloch,et al.  Autologous Adult Cortical Cell Transplantation Enhances Functional Recovery Following Unilateral Lesion of Motor Cortex in Primates: A Pilot Study , 2011, Neurosurgery.

[4]  T. Wannier,et al.  Behavioral Assessment of Manual Dexterity in Non-Human Primates , 2011, Journal of visualized experiments : JoVE.

[5]  J. Bloch,et al.  Representation of motor habit in a sequence of repetitive reach and grasp movements performed by macaque monkeys: Evidence for a contribution of the dorsolateral prefrontal cortex , 2013, Cortex.

[6]  I. Kermadi,et al.  Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. , 2000, Somatosensory & motor research.

[7]  J. Bloch,et al.  Primate adult brain cell autotransplantation produces behavioral and biological recovery in 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine‐induced parkinsonian St. Kitts monkeys , 2014, The Journal of comparative neurology.

[8]  M. Wiesendanger,et al.  Temporal Structure of a Bimanual Goal‐directed Movement Sequence in Monkeys , 1994, The European journal of neuroscience.

[9]  J. Tanji,et al.  Integration of temporal order and object information in the monkey lateral prefrontal cortex. , 2004, Journal of neurophysiology.

[10]  J. Bloch,et al.  Primate adult brain cell autotransplantation, a new tool for brain repair? , 2005, Experimental Neurology.

[11]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[12]  Brian Caffo,et al.  Effects of Working Memory Demand on Neural Mechanisms of Motor Response Selection and Control , 2013, Journal of Cognitive Neuroscience.

[13]  Hong Yu,et al.  Role of the basal ganglia and frontal cortex in selecting and producing internally guided force pulses , 2007, NeuroImage.

[14]  J. Tanji,et al.  Categorization of behavioural sequences in the prefrontal cortex , 2007, Nature.

[15]  Pooja Wasson,et al.  Predicting grip force amplitude involves circuits in the anterior basal ganglia , 2010, NeuroImage.

[16]  D Le Bihan,et al.  The Dorsolateral Prefrontal Cortex (dlpfc) Plays a Key Role in Working Memory (wm). yet Its Precise Contribution , 2022 .

[17]  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.

[18]  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..

[19]  I. Kermadi,et al.  Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. , 1998, Somatosensory & motor research.

[20]  Sam Silverman,et al.  THE RHESUS MONKEY , 1982 .

[21]  Hartwig R. Siebner,et al.  Brain activity is similar during precision and power gripping with light force: An fMRI study , 2008, NeuroImage.

[22]  Masataka Watanabe,et al.  Integration of cognitive and motivational context information in the primate prefrontal cortex. , 2007, Cerebral cortex.

[23]  I. Kermadi,et al.  Effects of reversible inactivation of the supplementary motor area (SMA) on unimanual grasp and bimanual pull and grasp performance in monkeys. , 1997, Somatosensory & motor research.

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

[25]  Hans Forssberg,et al.  Human brain activity in the control of fine static precision grip forces: an fMRI study , 2001, The European journal of neuroscience.

[26]  Richard S. J. Frackowiak,et al.  Multiple nonprimary motor areas in the human cortex. , 1997, Journal of neurophysiology.

[27]  H. Forssberg,et al.  Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. , 2001, Journal of neurophysiology.

[28]  J. Joseph,et al.  Prefrontal cortex and spatial sequencing in macaque monkey , 2004, Experimental Brain Research.

[29]  Michael Petrides,et al.  Frontal lobes and behaviour , 1994, Current Opinion in Neurobiology.

[30]  J. Sanes,et al.  Human brain activation accompanying explicitly directed movement sequence learning , 2001, Experimental Brain Research.

[31]  E. Rouiller,et al.  Distinction between hand dominance and hand preference in primates: a behavioral investigation of manual dexterity in nonhuman primates (macaques) and human subjects , 2013, Brain and behavior.

[32]  E. Rouiller,et al.  Variability of manual dexterity performance in non-human primates () , 2014 .

[33]  Carl R Olson,et al.  Rank signals in four areas of macaque frontal cortex during selection of actions and objects in serial order. , 2010, Journal of neurophysiology.

[34]  Hiroshi Kinoshita,et al.  Functional brain areas used for the lifting of objects using a precision grip: a PET study , 2000, Brain Research.

[35]  H. Freund,et al.  Clinical aspects of premotor function , 1985, Behavioural Brain Research.

[36]  Stephen C. Strother,et al.  Effects of Changes in Experimental Design on PET Studies of Isometric Force , 2001, NeuroImage.

[37]  E. M. Rouiller,et al.  Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys , 1999, Experimental Brain Research.

[38]  P. Magistretti,et al.  A Novel Method for In Vitro Production of Human Glial-Like Cells from Neurosurgical Resection Tissue , 2002, Laboratory Investigation.

[39]  P. Magistretti,et al.  Cryopreservation of human brain tissue allowing timely production of viable adult human brain cells for autologous transplantation. , 2003, Cryobiology.

[40]  David E Vaillancourt,et al.  Segregated and overlapping neural circuits exist for the production of static and dynamic precision grip force , 2011, Human brain mapping.

[41]  M Wiesendanger,et al.  Dexterity in adult monkeys following early lesion of the motor cortical hand area: the role of cortex adjacent to the lesion , 1998, The European journal of neuroscience.

[42]  B. Hyland,et al.  Neural activity of supplementary and primary motor areas in monkeys and its relation to bimanual and unimanual movement sequences , 1999, Neuroscience.

[43]  H. Kuypers,et al.  Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. , 1973, Brain : a journal of neurology.