Facilitation of neuronal activity in somatosensory and posterior parietal cortex during prehension

Abstract In order to study prehension in a reproducible manner, we trained monkeys to perform a task in which rectangular, spherical, and cylindrical objects were grasped, lifted, held, and lowered in response to visual cues. The animal’s hand movements were monitored using digital video, together with simultaneously recorded spike trains of neurons in primary somatosensory cortex (S-I) and posterior parietal cortex (PPC). Statistically significant task-related modulation of activity occurred in 78% of neurons tested in the hand area; twice as many cells were facilitated during object acquisition as were depressed. Cortical neurons receiving inputs from tactile receptors in glabrous skin of the fingers and palm, hairy skin of the hand dorsum, or deep receptors in muscles and joints of the hand modulated their firing rates during prehension in consistent and reproducible patterns. Spike trains of individual neurons differed in duration and amplitude of firing, the particular hand behavior(s) monitored, and their sensitivity to the shape of the grasped object. Neurons were classified by statistical analysis into groups whose spike trains were tuned to single task stages, spanned two successive stages, or were multiaction. The classes were not uniformly distributed in specific cytoarchitectonic fields, nor among particular somatosensory modalities. Sequential deformation of parts of the hand as the task progressed was reflected in successive responses of different members of this population. The earliest activity occurred in PPC, where 28% of neurons increased firing prior to hand contact with objects; such neurons may participate in anticipatory motor control programs. Activity shifted rostrally to S-I as the hand contacted the object and manipulated it. The shape of the grasped object had the strongest influence on PPC cells. The results suggest that parietal neurons monitor hand actions during prehension, as well as the physical properties of the grasped object, by shifting activity between populations responsive to hand shaping, grasping, and manipulatory behaviors.

[1]  B. Edin,et al.  Skin strain patterns provide kinaesthetic information to the human central nervous system. , 1995, The Journal of physiology.

[2]  Joaquín M. Fuster,et al.  Neuronal activity of somatosensory cortex in a cross-modal (visuo-haptic) memory task , 1997, Experimental Brain Research.

[3]  A. M. Smith,et al.  Primary motor cortical responses to perturbations of prehension in the monkey. , 1992, Journal of neurophysiology.

[4]  E V Evarts,et al.  Contrasts between activity of precentral and postcentral neurons of cerebral cortex during movement in the monkey. , 1972, Brain research.

[5]  V B Mountcastle,et al.  The parietal system and some higher brain functions. , 1995, Cerebral cortex.

[6]  R. Nelson Activity of monkey primary somatosensory cortical neurons changes prior to active movement , 1987, Brain Research.

[7]  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.

[8]  C. Leonard,et al.  Alterations of natural hand movements after interruption of fasciculus cuneatus in the macaque. , 1992, Somatosensory & motor research.

[9]  Edward V. Evarts,et al.  Pyramidal tract neurons in somatosensory cortex: central and peripheral inputs during voluntary movement , 1982, Brain Research.

[10]  J. Kalaska,et al.  Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements. , 1994, Journal of neurophysiology.

[11]  J COLE,et al.  Effects of small lesions in sensory cortex in trained monkeys. , 1954, Journal of neurophysiology.

[12]  Michio Tanaka,et al.  Postcentral neurons in hand region of area 2: their possible role in the form discrimination of tactile objects , 1978, Brain Research.

[13]  Michio Tanaka,et al.  Organization of the First Somatosensory Cortex for Manipulation of Objects: An Analysis of Behavioral Changes Induced by Muscimol Injection into Identified Cortical Loci of Awake Monkeys , 1991 .

[14]  Masahiro Sakamoto,et al.  Functional surface integration, submodality convergence, and tactile feature detection in area 2 of the monkey somatosensory cortex , 1985 .

[15]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[16]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[17]  M. Hulliger,et al.  The responses of afferent fibres from the glabrous skin of the hand during voluntary finger movements in man. , 1979, The Journal of physiology.

[18]  Masahiro Sakamoto,et al.  Deficits in manipulative behaviors induced by local injections of muscimol in the first somatosensory cortex of the conscious monkey , 1985, Brain Research.

[19]  Esther P. Gardner,et al.  Digital video: a tool for correlating neuronal firing patterns with hand motor behavior , 1998, Journal of Neuroscience Methods.

[20]  E P Gardner,et al.  Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys. , 1986, Journal of neurophysiology.

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

[23]  J. Abbs,et al.  Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. , 1991, Journal of neurophysiology.

[24]  H. Asanuma,et al.  Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. , 1993, Journal of neurophysiology.

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

[26]  E. Moberg The role of cutaneous afferents in position sense, kinaesthesia, and motor function of the hand. , 1983, Brain : a journal of neurology.

[27]  R. Johansson,et al.  Predictive feed-forward sensory control during grasping and manipulation in man , 1993 .

[28]  E P Gardner,et al.  Simulation of motion on the skin. V. Effect of stimulus temporal frequency on the representation of moving bar patterns in primary somatosensory cortex of monkeys. , 1992, Journal of neurophysiology.

[29]  H. Freund Disturbances of motor behaviour after parietal lobe lesions in the human , 1996 .

[30]  M Jeannerod,et al.  The hand and the object: the role of posterior parietal cortex in forming motor representations. , 1994, Canadian journal of physiology and pharmacology.

[31]  John W. Lane,et al.  Marking microelectrode penetrations with fluorescent dyes , 1996, Journal of Neuroscience Methods.

[32]  C. Leonard,et al.  Altered precision grasping in stumptail macaques after fasciculus cuneatus lesions. , 1992, Somatosensory & motor research.

[33]  M. Jeannerod The timing of natural prehension movements. , 1984, Journal of motor behavior.

[34]  Ageranioti-Bélanger Sa,et al.  Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task. II. Area 2 as compared to areas 3b and 1. , 1992 .

[35]  M Mishkin,et al.  Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys. , 1992, Journal of neurophysiology.

[36]  B. Edin Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. , 1992, Journal of neurophysiology.

[37]  Scott T. Grafton,et al.  Functional anatomy of pointing and grasping in humans. , 1996, Cerebral cortex.

[38]  J. Kalaska,et al.  Tactile activity in primate primary somatosensory cortex during active arm movements: correlation with receptive field properties. , 1994, Journal of neurophysiology.

[39]  J. Hyvärinen,et al.  Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. , 1974, Brain : a journal of neurology.

[40]  E. Fetz,et al.  Responses of identified cells in postcentral cortex of awake monkeys during comparable active and passive joint movements. , 1980, Journal of neurophysiology.

[41]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[42]  Yoshiaki Iwamura,et al.  Representation of reaching and grasping in the monkey postcentral gyrus , 1996, Neuroscience Letters.

[43]  E P Gardner,et al.  Spatial integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. , 1980, Journal of Neurophysiology.

[44]  S. Lederman The adaptive control of prehension. , 1994, Canadian journal of physiology and pharmacology.

[45]  C E Chapman,et al.  Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. , 1994, Canadian journal of physiology and pharmacology.

[46]  H. Sakata,et al.  Deficit of hand preshaping after muscimol injection in monkey parietal cortex , 1994, Neuroreport.

[47]  Masahiro Sakamoto,et al.  Postcentral neurons of alert monkeys activated by the contact of the hand with objects other than the monkey's own body , 1995, Neuroscience Letters.

[48]  J. Fuster,et al.  Mnemonic neuronal activity in somatosensory cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[49]  A P Batista,et al.  Posterior parietal areas specialized for eye movements (LIP) and reach (PRR) using a common coordinate frame. , 1998, Novartis Foundation symposium.

[50]  W A MacKay,et al.  Properties of reach-related neuronal activity in cortical area 7A. , 1992, Journal of neurophysiology.

[51]  H. Freund,et al.  Sensorimotor disturbances in patients with lesions of the parietal cortex. , 1989, Brain : a journal of neurology.

[52]  Marie-Claude Hepp-Reymond,et al.  Neuronal activity in the postcentral cortex related to force regulation during a precision grip task , 1986, Brain Research.

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