Transcranial Direct Current Stimulation (tDCS) Enhances the Excitability of Trigemino-Facial Reflex Circuits

BACKGROUND Transcranial direct current stimulation (tDCS) causes a tiny burning sensation through activation of local cutaneous trigeminal afferents. HYPOTHESIS Trigeminal sensory inputs from tDCS may generate excitability changes in the trigemino-facial reflex circuits. OBJECTIVES AND METHODS Sixteen healthy volunteers were submitted to 20 minutes tDCS sessions with two types of electrode-montage conditions: 1. Real vs Sham 'bi-hemispheric' tDCS (cathode/anode: C4/C3), for blinded assessment of effects, and 2. 'uni-hemispheric' tDCS (cathode/anode: Fp3/C3), for assessment of laterality of the effects. Supraorbital nerve stimuli were used to obtain blink reflexes before, during (10 minutes from onset) and after (30 minutes from onset) the tDCS session. Outcome measures were R2 habituation (R2H) to repeated stimuli, the blink reflex excitability recovery (BRER) to paired stimuli and the blink reflex inhibition by a prepulse (BRIP). RESULTS Real but not sham bi-hemispheric tDCS caused a significant decrease of R2H and leftward shift of BRER curve (p < 0.05 for all measures). The effects of uni-hemispheric tDCS on BRER and BRIP were larger on ipsilateral than on contralateral blink reflexes (p < 0.05). Excitability changes were still present 10 minutes after the end of stimulation in a lesser extent. CONCLUSIONS This study shows that 20 minute tDCS enhances the excitability of trigemino-facial reflex circuits. The finding of larger ipsilateral than contralateral effects suggests that sensitization through cutaneous trigeminal afferents adds on other possible mechanisms such as activation of cortico-nuclear or cortico-reticular connections.

[1]  N. Swerdlow,et al.  Prepulse inhibition of acoustic startle in rats after lesions of the pedunculopontine tegmental nucleus. , 1993, Behavioral neuroscience.

[2]  V. Weerdesteyn,et al.  Subcortical Structures in Humans Can Be Facilitated by Transcranial Direct Current Stimulation , 2014, PloS one.

[3]  Ian M Franks,et al.  Prepared Movements Are Elicited Early by Startle , 2004, Journal of motor behavior.

[4]  D. Reato,et al.  Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad , 2009, Brain Stimulation.

[5]  L. Cohen,et al.  Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation , 2006, Clinical Neurophysiology.

[6]  H. Kuypers.  CORTICOBULBAR CONNEXIONS TO THE PONS AND LOWER BRAIN-STEM IN MAN , 1958 .

[7]  M. Hallett,et al.  Transcranial magnetic brain stimulation modulates blepharospasm , 2010, Neurology.

[8]  B. Shahani,et al.  Assessing segmented excitability after acute rostral lesions , 1979, Neurology.

[9]  L. Bindman,et al.  The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long‐lasting after‐effects , 1964, The Journal of physiology.

[10]  E. Jankowska,et al.  Subcortical effects of transcranial direct current stimulation in the rat , 2013, The Journal of physiology.

[11]  J. Ison,et al.  Facilitation and inhibition of the human startle blink reflexes by stimulus anticipation. , 1990, Behavioral neuroscience.

[12]  J. Rothwell,et al.  Level of action of cathodal DC polarisation induced inhibition of the human motor cortex , 2003, Clinical Neurophysiology.

[13]  J. Valls-Solé,et al.  Enhanced gain of blink reflex responses to ipsilateral supraorbital nerve afferent inputs in patients with facial nerve palsy , 2001, Clinical Neurophysiology.

[14]  C. Eades.  Coronary atherosclerosis in renal hypertensive meat-fed rats. , 1966, Transactions of the New York Academy of Sciences.

[15]  G STRUCK,et al.  [Neurophysiology and morphology of the chronically isolated cortical islet in the cat: brain potentials and neuron activity of an isolated nerve cell population without afferent fibers]. , 1962, Archiv fur Psychiatrie und Nervenkrankheiten, vereinigt mit Zeitschrift fur die gesamte Neurologie und Psychiatrie.

[16]  M. Nitsche,et al.  Modulating cortico‐striatal and thalamo‐cortical functional connectivity with transcranial direct current stimulation , 2012, Human brain mapping.

[17]  J. Kimura,et al.  Blink reflex in patients with hemispheric cerebrovascular accident (CVA) Blink reflex in CVA , 1985, Journal of the Neurological Sciences.

[18]  M. Bikson,et al.  Electrodes for high-definition transcutaneous DC stimulation for applications in drug delivery and electrotherapy, including tDCS , 2010, Journal of Neuroscience Methods.

[19]  Alberto Leal,et al.  Comparing different electrode configurations using the 10-10 international system in tDCS: A finite element model analysis , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[20]  J. Molinuevo,et al.  Prepulse modulation of the startle reaction and the blink reflex in normal human subjects , 1999, Experimental Brain Research.

[21]  A. Berardelli,et al.  Metaplasticity of the human trigeminal blink reflex , 2010, The European journal of neuroscience.

[22]  M. Ridding,et al.  Transcranial electric and magnetic stimulation: technique and paradigms. , 2013, Handbook of clinical neurology.

[23]  M. Davis,et al.  Plasticity of the acoustic startle response in the acutely decerebrate rat. , 1977, Journal of comparative and physiological psychology.

[24]  C. Evinger,et al.  Effects of subthalamic deep brain stimulation on blink abnormalities of 6-OHDA lesioned rats. , 2015, Journal of neurophysiology.

[25]  N. Accornero,et al.  The orbicularis oculi response after hemispheral damage. , 1983, Journal of neurology, neurosurgery, and psychiatry.

[26]  Richard S. J. Frackowiak,et al.  How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? , 2005, The European journal of neuroscience.

[27]  G. Coppola,et al.  Reduced Habituation of Trigeminal Reflexes in Patients with Episodic Cluster Headache During Cluster Period , 2008, Cephalalgia : an international journal of headache.

[28]  J. Rothwell,et al.  Changes in blink reflex excitability after globus pallidus internus stimulation for dystonia , 2006, Movement disorders : official journal of the Movement Disorder Society.

[29]  J. Klmura.  Effect of hemispheral lesions on the contralateral blink reflex , 1974, Neurology.

[30]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[31]  D. Purpura,et al.  INTRACELLULAR ACTIVITIES AND EVOKED POTENTIAL CHANGES DURING POLARIZATION OF MOTOR CORTEX. , 1965, Journal of neurophysiology.

[32]  F. Valldeoriola,et al.  Single subthalamic nucleus deep brain stimuli inhibit the blink reflex in Parkinson's disease patients. , 2006, Brain : a journal of neurology.

[33]  Sunbin Song,et al.  Modifying somatosensory processing with non-invasive brain stimulation. , 2011, Restorative neurology and neuroscience.

[34]  P. Celnik,et al.  Modulation of Cerebellar Excitability by Polarity-Specific Noninvasive Direct Current Stimulation , 2009, The Journal of Neuroscience.

[35]  E. Granieri,et al.  Effect of slow rTMS of motor cortex on the excitability of the Blink Reflex: A study in healthy humans , 2009, Clinical Neurophysiology.

[36]  Walter Paulus,et al.  Transcranial direct current stimulation--update 2011. , 2011, Restorative neurology and neuroscience.

[37]  M. Hallett,et al.  Blepharospasm and the modulation of cortical excitability in primary and secondary motor areas , 2009, Neurology.

[38]  K. R. Peshori,et al.  Reflex Excitability Regulates Prepulse Inhibition , 2000, The Journal of Neuroscience.

[39]  F. Morrell.  EFFECT OF ANODAL POLARIZATION ON THE FIRING PATTERN OF SINGLE CORTICAL CELLS , 1961, Annals of the New York Academy of Sciences.

[40]  J. Jefferys,et al.  Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro , 2004, The Journal of physiology.

[41]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

[42]  A. Kossev,et al.  Unilateral reduction of the early and late blink reflex component in hemiparkinson syndrome. , 1982, Electroencephalography and clinical neurophysiology.

[43]  J. Rothwell,et al.  Patterned ballistic movements triggered by a startle in healthy humans , 1999, The Journal of physiology.

[44]  Elzbieta Jankowska,et al.  Evidence for long‐lasting subcortical facilitation by transcranial direct current stimulation in the cat , 2013, The Journal of physiology.

[45]  Abhishek Datta,et al.  Transcranial direct current stimulation in patients with skull defects and skull plates: High-resolution computational FEM study of factors altering cortical current flow , 2010, NeuroImage.

[46]  O. Carter,et al.  Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: A systematic review , 2015, Neuropsychologia.

[47]  C. Evinger,et al.  Long-Term Potentiation of the Human Blink Reflex , 2001, The Journal of Neuroscience.

[48]  L. Parra,et al.  Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects , 2013, The Journal of physiology.