Air-puff-induced facilitation of motor cortical excitability studied in patients with discrete brain lesions.

Air-puff stimulation applied to a fingertip is known to exert a location-specific facilitatory effect on the size of the motor evoked potentials elicited in hand muscles by transcranial magnetic stimulation. In order to clarify its nature and the pathway responsible for its generation, we studied 27 patients with discrete lesions in the brain (16, 9 and 2 patients with lesions in the cerebral cortex, thalamus and brainstem, respectively). Facilitation was absent in patients with lesions affecting the primary sensorimotor area, whereas it was preserved in patients with cortical lesions that spared this area. Facilitation was abolished with thalamic lesions that totally destroyed the nucleus ventralis posterolateralis (VPL), but was preserved with lesions that at least partly spared it. Lesions of the spinothalamic tract did not impair facilitation. The size of the N20-P25 component of the somatosensory evoked potential showed a mild correlation with the amount of facilitation. The facilitation is mainly mediated by sensory inputs that ascend the dorsal column and reach the cortex through VPL. These are fed into the primary motor area via the primary sensory area, especially its anterior portion, corresponding to Brodmann areas 3 and 1 (possibly also area 2), without involving other cortical regions. The spinothalamic tract and direct thalamic inputs into the motor cortex do not contribute much to this effect. Some patients could generate voluntary movements despite the absence of the facilitatory effect. The present method will enable us to investigate in humans the function of one of the somatotopically organized sensory feedback input pathways into the motor cortex, and will be useful in monitoring ongoing finger movements during object manipulation.

[1]  B Milner,et al.  Somatosensory thresholds--contrasting effects of postcentral-gyrus and posterior parietal-lobe excisions. , 1970, Archives of neurology.

[2]  K. Sakai,et al.  Excitation of the motor cortex associated with the E2 phase of cutaneous reflexes in man , 1994, Brain Research.

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

[4]  J. Jenner,et al.  Cutaneous reflex responses and their central nervous pathways studied in man , 1982, The Journal of physiology.

[5]  Allan H. Ropper,et al.  Evoked potentials in clinical medicine (second of two parts). , 1982 .

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

[7]  H. Asanuma,et al.  Organization of projection from the thalamic relay nuclei to the motor cortex in the cat. , 1974, Brain research.

[8]  K. Sakai,et al.  Clinical utility of magnetic corticospinal tract stimulation at the foramen magnum level. , 1995, Electroencephalography and clinical neurophysiology.

[9]  C. Woolsey,et al.  Motor performance of monkeys after bilateral partial and total cerebral decortications. , 1956, American journal of physical medicine.

[10]  J. Murphy,et al.  Spatial organization of precentral cortex in awake primates. III. Input-output coupling. , 1978, Journal of neurophysiology.

[11]  H Asanuma,et al.  Experiments on functional role of peripheral input to motor cortex during voluntary movements in the monkey. , 1984, Journal of neurophysiology.

[12]  P. Wall,et al.  A clinical and neurophysiological study of a patient with an extensive transection of the spinal cord sparing only a part of one anterolateral quadrant. , 1996, Brain : a journal of neurology.

[13]  P E Roland,et al.  Somatotopical tuning of postcentral gyrus during focal attention in man. A regional cerebral blood flow study. , 1981, Journal of neurophysiology.

[14]  M. Wiesendanger,et al.  The Supplementary Motor Area in the Light of Recent Investigations , 1984 .

[15]  P. Strick Light microscopic analysis of the cortical projection of the thalamic ventrolateral nucleus in the cat. , 1973, Brain research.

[16]  J C Rothwell,et al.  Effect of digital nerve stimuli on responses to electrical or magnetic stimulation of the human brain. , 1992, The Journal of physiology.

[17]  M. Tiengo,et al.  [Short latency somatosensory evoked potentials. Methodologic considerations and interpretations]. , 1985, Minerva anestesiologica.

[18]  H. Yumiya,et al.  Receptive fields of thalamic neurons projecting to the motor cortex in the cat , 1979, Brain Research.

[19]  George D.M Gordon,et al.  Active touch: The mechanism of recognition of objects by manipulation, a multi-disciplinary approach : proceedings of a symposium held at Beaune, France, July 1977 , 1978 .

[20]  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.

[21]  H. Asanuma,et al.  Importance of the projection from the sensory to the motor cortex for recovery of motor function following partial thalamic lesion in the monkey , 1987, Brain Research.

[22]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[23]  B. Day,et al.  Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. , 1989, The Journal of physiology.

[24]  V. Mountcastle,et al.  THE FUNCTIONAL PROPERTIES OF VENTROBASAL THALAMIC NEURONSSTUDIED IN UNANESTHETIZED MONKEYS. , 1963, Journal of neurophysiology.

[25]  R. Dejong,et al.  THE NEUROLOGIC EXAMINATION , 1959 .

[26]  M. Swash,et al.  The Motor Cortex , 1990 .

[27]  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.

[28]  M. Posner,et al.  Attentional Mechanisms and Conscious Experience , 1992 .

[29]  Ichiro Kanazawa,et al.  Primary motor cortex isolation: complete paralysis with preserved primary motor cortex , 1998, Journal of the Neurological Sciences.

[30]  B. Whitsel,et al.  Effects of spinal dorsal column transection on the response of monkey anterior parietal cortex to repetitive skin stimulation. , 1996, Cerebral cortex.

[31]  H Asanuma,et al.  Functional role of corticoperipheral loop circuits during voluntary movements in the monkey: a preferential bias theory , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Alan C. Evans,et al.  Attention modulates somatosensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography , 1991, Annals of neurology.

[33]  I. Kanazawa,et al.  Input-output organization in the hand area of the human motor cortex. , 1995, Electroencephalography and clinical neurophysiology.

[34]  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.

[35]  Edward G. Jones,et al.  Connectivity of the Primate Sensory-Motor Cortex , 1986 .

[36]  A. Iriki,et al.  Attention-induced neuronal activity in the monkey somatosensory cortex revealed by pupillometrics , 1996, Neuroscience Research.

[37]  W. Chambers,et al.  The effect of postcentral cortical lesions on motor responses to sudden upper limb displacements in monkeys , 1975, Brain Research.

[38]  J. Stephens,et al.  The reflex responses of single motor units in human first dorsal interosseous muscle following cutaneous afferent stimulation. , 1980, The Journal of physiology.

[39]  T. R Fisher,et al.  Active touch. The mechanism of recognition of objects by manipulation. A multi-disciplinary approach: Edited by George Gordon. Pp. 275. Pergamon Press, Oxford, 1978. Hard cover £19.50, flexi cover £11.00 , 1979 .

[40]  A. Milner,et al.  Neuropsychology of Consciousness , 2019, Frontiers Research Topics.

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