The effects of cerebellar stimulation on the motor cortical excitability in neurological disorders: A review

The cerebellum regulates execution of skilled movements through neural connections with the primary motor cortex. A main projection from the cerebellum to the primary motor cortex is a disynaptic excitatory pathway relayed at the ventral thalamus. This dentatothalamocortical pathway receives inhibitory inputs from Purkinje cells of the cerebellar cortex. These pathways (cerebellothalamocortical pathways) have been characterized extensively using cellular approaches in animals. Advances in non-invasive transcranial activation of neural structures using electrical and magnetic stimulation have allowed us to investigate these neural connections in humans. This review summarizes various studies of the cerebellothalamo-cortical pathway in humans using current transcranial electrical and magnetic stimulation techniques. We studied effects on motor cortical excitability elicited by electrical or magnetic stimulation over the cerebellum by recording surface electromyographic (EMG) responses from the first dorsal interosseous (FDI) muscle. Magnetic stimuli were given with a round or figure eight coil (test stimulation) for primary motor cortical activation. For cerebellar stimulation, we gave high-voltage electrical stimuli or magnetic stimuli through a cone-shaped coil ipsilateral to the surface EMG recording (conditioning stimulation). We examined effects of interstimulus intervals (ISIs) with randomized condition-test paradigm, using a test stimulus given preceded by a conditioning stimulus by ISIs of several milliseconds. We demonstrated significant gain of EMG responses at an ISI of 3 ms (facilitatory effect) and reduced responses starting at 5 ms, which lasted 3–7 ms (inhibitory effect). We applied this method to patients with ataxia and showed that the inhibitory effect was only absent in patients with a lesion at cerebellar efferent pathways or dentatothalamocortical pathway. These results imply that this method activates the unilateral cerebellar structures. We confirmed facilitatory and inhibitory natures of cerebellothala-mocortical pathways in humans. We can differentiate ataxia attributable to somewhere in the cerebello-thalamo-cortical pathways from that caused by other pathways.

[1]  Brian L. Day,et al.  Different sites of action of electrical and magnetic stimulation of the human brain , 1987, Neuroscience Letters.

[2]  I. L. Freeston,et al.  CLINICAL EVALUATION OF CONDUCTION TIME MEASUREMENTS IN CENTRAL MOTOR PATHWAYS USING MAGNETIC STIMULATION OF HUMAN BRAIN , 1986, The Lancet.

[3]  I. Kanazawa,et al.  Suppression of motor cortical excitability by electrical stimulation over the cerebellum in Fisher's syndrome. , 1994, Journal of neurology, neurosurgery, and psychiatry.

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

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

[6]  Y Shinoda,et al.  Cerebellar input to corticothalamic neurons in layers V and VI in the motor cortex , 1997, Neuroscience Research.

[7]  K. Sakai,et al.  Magnetic stimulation over the cerebellum in patients with ataxia. , 1997, Electroencephalography and clinical neurophysiology.

[8]  R. Hanajima,et al.  Magnetic stimulation over the cerebellum in humans , 1995, Annals of neurology.

[9]  P. Strick,et al.  The Organization of Cerebellar and Basal Ganglia Outputs to Primary Motor Cortex as Revealed by Retrograde Transneuronal Transport of Herpes Simplex Virus Type 1 , 1999, The Journal of Neuroscience.

[10]  J. Houk,et al.  Functional connectivity between cerebellum and primary motor cortex in the awake monkey. , 2000, Journal of neurophysiology.

[11]  K. Nakamura,et al.  Electrical stimulation of the cerebellum normally suppresses motor cortical excitability in a patient with ataxia due to a lesion of the middle cerebellar peduncle. , 1995, European neurology.

[12]  R. Hanajima,et al.  Magnetic stimulation of corticospinal pathways at the foramen magnum level in humans , 1994, Annals of neurology.

[13]  Ichiro Kanazawa,et al.  Interhemispheric facilitation of the hand area of the human motor cortex , 1993, Neuroscience Letters.

[14]  V. Amassian,et al.  Physiological basis of motor effects of a transient stimulus to cerebral cortex. , 1987, Neurosurgery.

[15]  I. Kanazawa,et al.  Interhemispheric facilitation of the hand motor area in humans , 2001, The Journal of physiology.

[16]  V. Amassian,et al.  Motor cortical and other cortical interneuronal networks that generate very high frequency waves. , 2003, Supplements to Clinical neurophysiology.

[17]  K. Sasaki,et al.  Electrophysiological studies on the cerebellocerebral projections in monkeys , 1976, Experimental Brain Research.

[18]  S. Tsuji,et al.  Cerebellar stimulation in acute cerebellar ataxia , 2001, Clinical Neurophysiology.

[19]  H. Jörntell,et al.  Functional organization of climbing fibre projection to the cerebellar anterior lobe of the rat , 2000, The Journal of physiology.

[20]  B. Day,et al.  Modulation of motor cortical excitability by electrical stimulation over the cerebellum in man. , 1991, The Journal of physiology.

[21]  C D Marsden,et al.  Percutaneous electrical stimulation of corticospinal pathways at the level of the pyramidal decussation in humans , 1991, Annals of neurology.

[22]  M. Molinari,et al.  Cerebro-cerebellar interactions in man: neurophysiological studies in patients with focal cerebellar lesions. , 1994, Electroencephalography and clinical neurophysiology.

[23]  K. Sakai,et al.  Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight-shaped coil , 2006, Experimental Brain Research.

[24]  Y. Ugawa,et al.  Chapter 13 – Cerebellar Stimulation in Normal Subjects and Ataxic Patients , 2005 .

[25]  K. Sakai,et al.  Paired‐pulse magnetic stimulation of the human motor cortex: differences among I waves , 1998, The Journal of physiology.

[26]  G. Allen,et al.  Cerebrocerebellar communication systems. , 1974, Physiological reviews.

[27]  R. Post,et al.  Transcranial magnetic stimulation: a neuropsychiatric tool for the 21st century. , 1996, The Journal of neuropsychiatry and clinical neurosciences.

[28]  M. Steriade.  Two channels in the cerebellothalamocortical system , 1995, The Journal of comparative neurology.

[29]  Y Shinoda,et al.  Thalamocortical organization in the cerebello-thalamo-cortical system. , 1993, Cerebral cortex.

[30]  J C Rothwell,et al.  Suppression of motor cortical excitability by electrical stimulation over the cerebellum in ataxia , 1994, Annals of neurology.

[31]  I. Kanazawa,et al.  Facilitatory effect on the motor cortex by electrical stimulation over the cerebellum in humans , 2004, Experimental Brain Research.