Neural generators of early cortical somatosensory evoked potentials in the awake monkey.

Controversy continues to exist regarding the generators of the initial cortical components of the somatosensory evoked potential (SEP). This issue was explored by detailed epidural and intracortical mapping of somatosensory evoked activity in Old World monkeys. In depth recordings, 3 complementary procedures were utilized: (1) the intracortical and subcortical distribution of SEPs was determined from approximately 4000 locations; (2) concomitant profiles of multiple unit activity (MUA) were recorded as an estimate of local action potential profiles; (3) 1-dimensional calculations of current source density (CSD) were used to outline the timing and pattern of regional transmembrane current flow. Our analysis confirms the participation of multiple cortical areas, located on either side of the central sulcus, in the generation of the initial cortical SEP components. Earliest activity P10, was localized to area 3, followed within milliseconds by activation of areas 1, 2 (P12), and 4 (P13). In SI (Brodmann's areas 3, 1 and 2), the initial SEP components reflect the depolarization of lamina 4 stellate cells and the subsequent activation of adjacent pyramidal cells in laminae 3 and 5. The genesis of later cortical components (P20, N45) represents the composite of activity distributed across multiple cortical laminae and the interaction of overlapping excitatory and inhibitory events. These findings have direct implications for the clinical interpretation of SEP waveforms.

[1]  C. G. Phillips,et al.  Inputs from low threshold muscle and cutaneous afferents of hand and forearm to areas 3a and 3b of baboon's cerebral cortex. , 1976, The Journal of physiology.

[2]  A. Starr,et al.  Mechanically and electrically evoked somatosensory potentials in human: scalp and neck distributions of short latency components. , 1981, Electroencephalography and clinical neurophysiology.

[3]  H. Vaughan,et al.  Topography and intracranial sources of somatosensory evoked potentials in the monkey. II. Cortical components. , 1981, Electroencephalography and clinical neurophysiology.

[4]  Emanuel Donchin,et al.  Average evoked potentials - Methods, results, and evaluations , 1969 .

[5]  R P Lesser,et al.  Cortical generators of somatosensory evoked potentials to median nerve stimulation , 1987, Neurology.

[6]  G. Cheron,et al.  Non-cephalic reference recording of early somatosensory potentials to finger stimulation in adult or aging normal man: differentiation of widespread N18 and contralateral N20 from the prerolandic P22 and N30 components. , 1981, Electroencephalography and clinical neurophysiology.

[7]  H. Vaughan,et al.  A new multielectrode array for the simultaneous recording of field potentials and unit activity. , 1981, Electroencephalography and clinical neurophysiology.

[8]  T. Suenaga,et al.  Volume conduction of the parietal N20 potential to the prerolandic frontal area. , 1990, Brain : a journal of neurology.

[9]  F Mauguiere,et al.  Separate generators with distinct orientations for N20 and P22 somatosensory evoked potentials to finger stimulation? , 1986, Electroencephalography and clinical neurophysiology.

[10]  M Wiesendanger,et al.  Responses of neurones in motor cortex and in area 3A to controlled stretches of forelimb muscles in cebus monkeys. , 1975, The Journal of physiology.

[11]  K Takeda,et al.  SEPs in two patients with localized lesions of the postcentral gyrus. , 1991, Electroencephalography and clinical neurophysiology.

[12]  S. Tsuji,et al.  Topography of somatosensory evoked potentials to median nerve stimulation in patients with cerebral lesions. , 1988, Electroencephalography and clinical neurophysiology.

[13]  R P Lesser,et al.  Evoked Potentials in Cortical Localization , 1986, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[14]  E. G. Jones,et al.  Differential thalamic relationships of sensory‐motor and parietal cortical fields in monkeys , 1979, The Journal of comparative neurology.

[15]  Spielholz Ni Intraoperative monitoring using somato-sensory evoked potentials: a brief overview. , 1994 .

[16]  J. H. Kaas,et al.  Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1 , 1990, Brain Research.

[17]  T. Landis,et al.  Dissociation of frontal and parietal components of somatosensory evoked potentials in severe head injury. , 1993, Electroencephalography and clinical neurophysiology.

[18]  C. C. Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. , 1989, Journal of neurophysiology.

[19]  S. Tsuji,et al.  Frontal distribution of early cortical somatosensory evoked potentials to median nerve stimulation. , 1988, Electroencephalography and clinical neurophysiology.

[20]  J Kimura,et al.  Short latency somatosensory evoked potentials following median nerve stimulation in man. , 1980, Electroencephalography and clinical neurophysiology.

[21]  G. Pfurtscheller Handbook of electroencephalography and clinical neurophysiology , 1978 .

[22]  J E Desmedt,et al.  Bit-mapped color imaging of human evoked potentials with reference to the N20, P22, P27 and N30 somatosensory responses. , 1987, Electroencephalography and clinical neurophysiology.

[23]  C C Wood,et al.  Electrical sources in human somatosensory cortex: identification by combined magnetic and potential recordings. , 1985, Science.

[24]  C. C. Wood,et al.  Cortical somatosensory evoked potentials. II. Effects of excision of somatosensory or motor cortex in humans and monkeys. , 1991, Journal of neurophysiology.

[25]  Mitchell Steinschneider,et al.  Intracranial generators of event-related potentials in the monkey , 1986 .

[26]  C. Nicholson,et al.  Experimental optimization of current source-density technique for anuran cerebellum. , 1975, Journal of neurophysiology.

[27]  R. Porter,et al.  What is area 3a? , 1980, Brain Research Reviews.

[28]  C. Schroeder,et al.  The Genesis of Cortical Event-Related Potentials: Excitatory and Inhibitory Contributions , 1993 .

[29]  J. Stein Progress in clinical neurophysiology Vol. 4. Cerebral motor control in man: Long loop mechanisms. Edited by J. E. Desmedt. S. Karger, Basel, 1979, 394 pp. $70.75 , 1980, Neuropsychologia.

[30]  M Hämäläinen,et al.  Early deflections of cerebral magnetic responses to median nerve stimulation. , 1989, Electroencephalography and clinical neurophysiology.

[31]  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.

[32]  A. Wyler,et al.  Somatosensory evoked potentials after removal of somatosensory cortex in man. , 1986, Electroencephalography and Clinical Neurophysiology.

[33]  C. E. Schroeder,et al.  Contribution of extrastriate area V4 to the surface-recorded flash VEP in the awake macaque , 1994, Vision Research.

[34]  J. B. Preston,et al.  Responses of cortical neurons (areas 3a and 4) to ramp stretch of hindlimb muscles in the baboon. , 1976, Journal of neurophysiology.

[35]  E P Gardner,et al.  Somatosensory evoked potentials (SEPs) and cortical single unit responses elicited by mechanical tactile stimuli in awake monkeys. , 1984, Electroencephalography and clinical neurophysiology.

[36]  J. Kimura,et al.  SHORT‐LATENCY SOMATOSENSORY EVOKED POTENTIALS FOLLOWING MEDIAN NERVE STIMULATION , 1980 .

[37]  R P Lesser,et al.  Cortical somatosensory evoked potentials in response to hand stimulation. , 1983, Journal of neurosurgery.

[38]  M. Fukuda,et al.  Localization of dipole by boundary element method in three dimensional reconstructed monkey brain , 1994, Brain Research Bulletin.

[39]  Dipole tracing of monkey somatosensory evoked potentials , 1994, Brain Research Bulletin.

[40]  Truett Allison SCALP AND CORTICAL RECORDINGS OF INITIAL SOMATOSENSORY CORTEX ACTIVITY TO MEDIAN NERVE STIMULATION IN MAN * , 1980 .

[41]  G Cheron,et al.  Somatosensory evoked potentials to finger stimulation in healthy octogenarians and in young adults: wave forms, scalp topography and transit times of parietal and frontal components. , 1980, Electroencephalography and clinical neurophysiology.

[42]  Hiroshi Shibasaki,et al.  Somatosensory evoked potentials Diagnostic criteria and abnormalities in cerebral lesions , 1977, Journal of the Neurological Sciences.

[43]  C C Wood,et al.  Cortical somatosensory evoked potentials. I. Recordings in the monkey Macaca fascicularis. , 1991, Journal of neurophysiology.

[44]  T Allison,et al.  The scalp topography of human somatosensory and auditory evoked potentials. , 1977, Electroencephalography and clinical neurophysiology.

[45]  P. Furlong,et al.  Augmented P22-N31 SEP component in a patient with a unilateral space occupying lesion. , 1993, Electroencephalography and clinical neurophysiology.

[46]  F Mauguière,et al.  Astereognosis and dissociated loss of frontal or parietal components of somatosensory evoked potentials in hemispheric lesions. Detailed correlations with clinical signs and computerized tomographic scanning. , 1983, Brain : a journal of neurology.

[47]  C. Schroeder,et al.  Laminar analysis of bicuculline-induced epileptiform activity in area 17 of the awake macaque , 1990, Brain Research.

[48]  F Mauguière,et al.  Focal capsular vascular lesions can selectively deafferent the prerolandic or the parietal cortex: Somatosensory evoked potentials evidence , 1991, Annals of neurology.