Comparison of neuronal firing rates in somatosensory and posterior parietal cortex during prehension

Abstract. To evaluate their functional roles during prehension, single-unit recordings were made in the hand area of primary somatosensory areas 3b, 1 and 2 (S-I) and posterior parietal areas 5 and 7 (PPC) of the same animal. Response profiles of mean firing rate during performance of a multistage reach, grasp, and lift task were analyzed to determine the period(s) of peak firing and to measure statistically significant rises or falls in rate compared with baseline. We used the peak firing stage(s) to subdivide the population into classes tuned to single actions or two successive stages, or into multiaction groups that had sustained facilitation (BT) or inhibition (GI) during hand-object interactions. Four times as many neurons fired at peak rates during acquisition stages (approach, contact, grasp) than upon release, and their firing rates were higher. Grasping evoked the strongest responses, as grasp-tuned neurons had the highest peak rates in the population; BT, contact-grasp, and grasp-lift cells also fired maximally in the grasp stage. Grasping also coincided with maximal inhibition of GI cells, as well as of neurons tuned to approach or relaxation of grasp. Holding evoked the lowest mean rates, and had the fewest tuned cells. S-I and PPC showed significant differences in behaviors evoking peak firing as well as facilitation and inhibition; these correlated with input modalities in each area. Hand contact with the object and positioning of the fingers for grasp was the most strongly represented behavior in anterior S-I, where 61% received tactile inputs from glabrous skin. Nearly 60% were facilitated at contact, 38% fired at peak rates, and 10% were inhibited; release of grasp evoked peak firing in only 5% of 3b-1 neurons. In posterior S-I, where proportions of tactile and deep inputs were similar, positioning and grasping elicited peak responses in 38% and 31%, respectively; 80% were facilitated or inhibited during grasping. During lift and hold, inhibition rose to 43%, while excitation declined under 10%. PPC had the highest proportions firing at peak rates during hand preshaping before contact (28%) and had the most facilitated responses (38%) in this stage. Only 10% fired at peak rates during grasping. During later manipulatory actions, proportions of facilitated and inhibited responses in PPC were similar to those in posterior S-I. The data support models in which PPC plans hand movements during prehension rather than guiding their execution. Sensory monitoring of hand-object interaction occurs in S-I, where cells sense specific hand behaviors, signal stage completion, enable error correction, and may update grasp programs formulated in PPC. The results are discussed in relation to those obtained from lesion studies in humans.

[1]  A. M. Smith,et al.  The effects of muscimol inactivation of small regions of motor and somatosensory cortex on independent finger movements and force control in the precision grip , 1999, Experimental Brain Research.

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

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

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

[5]  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 .

[6]  J. Ghika,et al.  Parietal motor syndrome: A clinical description in 32 patients in the acute phase of pure parietal strokes studied prospectively , 1998, Clinical Neurology and Neurosurgery.

[7]  H. Sakata,et al.  The TINS Lecture The parietal association cortex in depth perception and visual control of hand action , 1997, Trends in Neurosciences.

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

[9]  C Dohle,et al.  Human anterior intraparietal area subserves prehension , 1998, Neurology.

[10]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

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

[14]  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.

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

[16]  R. J. Seitz,et al.  A parieto-premotor network for object manipulation: evidence from neuroimaging , 1999, Experimental Brain Research.

[17]  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.

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

[19]  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.

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

[21]  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.

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

[23]  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.

[24]  R. LaMotte,et al.  Defects in accuracy of reaching after removal of posterior parietal cortex in monkeys , 1978, Brain Research.

[25]  H. Sakata,et al.  Neural representation of three-dimensional features of manipulation objects with stereopsis , 1999, Experimental Brain Research.

[26]  P Jenmalm,et al.  Visual and Somatosensory Information about Object Shape Control Manipulative Fingertip Forces , 1997, The Journal of Neuroscience.

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

[28]  T Brochier,et al.  Neuronal activity in somatosensory cortex of monkeys using a precision grip. I. Receptive fields and discharge patterns. , 1999, Journal of neurophysiology.

[29]  J. Fuster,et al.  Visuo-tactile cross-modal associations in cortical somatosensory cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[31]  H. Freund,et al.  Force regulation is deficient in patients with parietal lesions: a system-analytic approach. , 1998, Electroencephalography and clinical neurophysiology.

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

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

[34]  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.

[35]  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.

[36]  Soumya Ghosh,et al.  Facilitation of neuronal activity in somatosensory and posterior parietal cortex during prehension , 1999, Experimental Brain Research.

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

[38]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[39]  A. Georgopoulos Current issues in directional motor control , 1995, Trends in Neurosciences.

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

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

[42]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[43]  R S Johansson,et al.  Sensory input and control of grip. , 1998, Novartis Foundation symposium.

[44]  Esther P. Gardner,et al.  Depression of neuronal firing rates in somatosensory and posterior parietal cortex during object acquisition in a prehension task , 2000, Experimental Brain Research.

[45]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[46]  A. M. Smith,et al.  Friction, not texture, dictates grip forces used during object manipulation. , 1996, Journal of neurophysiology.

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