Human brain activity in the control of fine static precision grip forces: an fMRI study

Dexterous manipulation of delicate objects requires exquisite control of fingertip forces. We have used functional magnetic resonance imaging to identify brain regions involved in the skilful scaling of these forces when normal human subjects (n = 8) held with precision grip a small object (weight 200 g) in the dominant right hand. In one condition, they used their normal, automatically scaled grip force. The object was held gently in a second condition; the isometric grip force was maintained just above the critical level at which the object would have slipped. In a third condition, the force was increased to hold the object with a more firm grip. The supplementary and cingulate motor areas were significantly more active during the gentle force condition than during either of the other conditions in all subjects, despite weaker contractions of the hand muscles. In addition, the left primary sensorimotor cortex, the ventral premotor cortex and the left posterior parietal cortex were more strongly activated during gentle than during normal grasping. These novel results suggest that these regions are specifically involved in dexterous scaling of fingertip forces during object manipulation.

[1]  The supplementary motor area modulates perturbation-evoked discharges of neurones in the precentral motor cortex , 1986, Neuroscience Letters.

[2]  B. Weber,et al.  Context-dependent force coding in motor and premotor cortical areas , 1999, Experimental Brain Research.

[3]  R. Passingham,et al.  Relation between cerebral activity and force in the motor areas of the human brain. , 1995, Journal of neurophysiology.

[4]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[5]  A. M. Smith,et al.  Comparison of the neuronal activity in the SMA and the ventral cingulate cortex during prehension in the monkey. , 1997, Journal of neurophysiology.

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

[7]  G. Thickbroom,et al.  Isometric force-related activity in sensorimotor cortex measured with functional MRI , 1998, Experimental Brain Research.

[8]  Duane E. Haines,et al.  Federation of European Neuroscience Societies 2000 meeting , 2000 .

[9]  K. Zilles,et al.  Functions and structures of the motor cortices in humans , 1996, Current Opinion in Neurobiology.

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

[11]  M. Hepp-Reymond,et al.  Contrasting properties of monkey somatosensory and motor cortex neurons activated during the control of force in precision grip. , 1991, Journal of neurophysiology.

[12]  G. Thickbroom,et al.  Differences in functional magnetic resonance imaging of sensorimotor cortex during static and dynamic finger flexion , 1999, Experimental Brain Research.

[13]  Lemon Rn,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993 .

[14]  S S Hsiao,et al.  Effects of selective attention on spatial form processing in monkey primary and secondary somatosensory cortex. , 1993, Journal of neurophysiology.

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

[16]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[17]  Roland S. Johansson,et al.  Sensory Control of Dexterous Manipulation in Humans , 1996 .

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

[19]  Daniel Bourbonnais,et al.  Interaction between forced grasping and a learned precision grip after ablation of the supplementary motor area , 1981, Brain Research.

[20]  Karl J. Friston,et al.  Quantitative Comparison of Functional Magnetic Resonance Imaging with Positron Emission Tomography Using a Force-Related Paradigm , 1996, NeuroImage.

[21]  A. M. Smith,et al.  Primary motor cortical activity related to the weight and texture of grasped objects in the monkey. , 1992, Journal of neurophysiology.

[22]  P H Ellaway,et al.  Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. , 1994, The Journal of physiology.

[23]  M Honda,et al.  Activities of the Primary and Supplementary Motor Areas Increase in Preparation and Execution of Voluntary Muscle Relaxation: An Event-Related fMRI Study , 1999, The Journal of Neuroscience.

[24]  Marie-Claude Hepp-Reymond,et al.  3 – Precision Grip in Humans: Temporal and Spatial Synergies , 1996 .

[25]  R N Lemon,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993, Experimental physiology.

[26]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[27]  R. Lemon,et al.  Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. , 1993, Journal of neurophysiology.

[28]  G. R. Crelier,et al.  Activation in multiple cortical regions in a visually cued grip force task: An event-related fMRI study , 2000, NeuroImage.

[29]  H Forssberg,et al.  IMPAIRED ANTICIPATORY CONTROL OF ISOMETRIC FORCES DURING GRASPING BY CHILDREN WITH CEREBRAL PALSY , 1992, Developmental medicine and child neurology.

[30]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[31]  J Tanji,et al.  Input organization of distal and proximal forelimb areas in the monkey primary motor cortex: A retrograde double labeling study , 1993, The Journal of comparative neurology.

[32]  Christian Bohm,et al.  Somatosensory Discrimination of Shape: Tactile Exploration and Cerebral Activation , 1991, The European journal of neuroscience.

[33]  H. Sakata,et al.  Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. , 1995, Cerebral cortex.

[34]  Karl J. Friston,et al.  Regional cerebral blood flow during voluntary arm and hand movements in human subjects. , 1991, Journal of neurophysiology.

[35]  J. Hermsdörfer,et al.  Disturbed grip-force control following cerebral lesions. , 1996, Journal of hand therapy : official journal of the American Society of Hand Therapists.

[36]  M. Preul The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

[37]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[38]  M. Hepp-Reymond,et al.  Force-related neuronal activity in two regions of the primate ventral premotor cortex. , 1994, Canadian journal of physiology and pharmacology.

[39]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  J Hyvärinen,et al.  Influence of attentive behavior on neuronal responses to vibration in primary somatosensory cortex of the monkey. , 1980, Journal of neurophysiology.

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

[42]  M. Dimitrijevic,et al.  Characteristics of spinal cord-evoked responses in man. , 1980, Applied neurophysiology.

[43]  R. Lemon,et al.  Corticospinal neurons with a special role in precision grip , 1983, Brain Research.

[44]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[45]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.

[46]  M. Honda,et al.  Both primary motor cortex and supplementary motor area play an important role in complex finger movement. , 1993, Brain : a journal of neurology.

[47]  K. Stephan,et al.  Cerebral midline structures in bimanual coordination , 1999, Experimental Brain Research.

[48]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.