Abstract
Objective
Tourette syndrome (TS) is a neurobehavioral disorder characterized by motor and vocal
tics. Simple tics are purposeless involuntary movements that spontaneously resolve
during middle adolescence. Complex tics appear to be semi-voluntary movements that
may become intractable when associated with obsessive–compulsive disorder (OCD). Sensory
tics or urges preceded by tics suggest sensorimotor processing impairment in TS. We
aimed to clarify its pathophysiology by exploring the pre-movement gating (attenuation)
of somatosensory evoked potentials (SEPs).
Methods
We examined 42 patients (aged 9–48 years), 4 of whom underwent follow-up assessment,
along with 19 healthy controls. We defined patients with only simple tics as TS-S
and patients with complex tics as TS-C. Pre-movement gating of SEPs was assessed using
a previously described method. Frontal N30 (FrN30) amplitudes were compared between
pre-movement and resting states. The gating ratio of pre-movement/resting amplitude
of the FrN30 component was assessed: the larger the ratio, the less the gating.
Results
The gating ratio for TS-C patients was larger than that of TS-S patients and healthy
controls, but a statistical difference between TS-S and TS-C appeared after 15 years
and over (p < 0.001). There were no significant differences in the gating ratio between TS-S
patients and healthy controls. The gating ratio was related to the severity of OCD
(p < 0.05).
Conclusion
Sensorimotor processing was preserved for simple tics but impaired in complex tics,
specifically after middle adolescence. Our study supports an age-dependent dysfunction
of both motor and non-motor cortico-striato-thalamo-cortical circuits in complex tics.
SEP gating seems promising as a tool for assessing age-dependent sensorimotor disintegration
in TS.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Brain and DevelopmentAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Course of tic severity in Tourette syndrome: the first two decades.Pediatrics. 1998; 102: 14-19
- The neurophysiology of Tourette syndrome.Adv Neurol. 1982; 35: 105-114
- Bereitschaftspotential in tic disorders: a preliminary observation.Neurol India. 2002; 50: 487-489
- Neurobiological substrates of Tourette’s disorder.J Child Adolesc Psychopharmacol. 2010; 20: 237-247
- Putting the pieces together in Gilles de la Tourette syndrome: exploring the link between clinical observations and the biological basis of dysfunction.Brain Topogr. 2017; 30: 3-29
- Premonitory sensory phenomenon in Tourette’s syndrome.Mov Disord. 2003; 18: 1530-1533
- Sensory phenomena in Tourette syndrome: their role in symptom formation and treatment.Curr Dev Disord Rep. 2014; 1: 245-251
- Sensory aspects of movement disorders.Lancet Neurol. 2014; 13: 100-112
- Altered structural connectivity of cortico-striato-pallido-thalamic networks in Gilles de la Tourette syndrome.Brain. 2015; 138: 472-482
- ‘Gating’ of somatosensory evoked potentials begins before the onset of voluntary movement in man.Brain Res. 1985; 348: 183-186
- The modulation of somatosensory evoked potentials during the foreperiod of a forewarned reaction time task.Electroencephalogr Clin Neurophysiol. 1993; 88: 105-117
- Pre-movement gating of short-latency somatosensory evoked potentials.Neuroreport. 1999; 10: 2457-2460
- Abnormal premovement gating of somatosensory input in writer’s cramp.Brain. 2000; 123: 1813-1829
- Centrifugal and centripetal mechanisms involved in the ‘gating’ of cortical SEPSs during movement.Electroencephalogr Clin Neurophysiol. 1989; 74: 36-45
- Pre-movement gating of somatosensory evoked potentials in Segawa disease.Brain Dev. 2016; 38: 68-75
- Bit-mapped somatosensory evoked potentials and muscular reflex responses in man: comparative analysis in different experimental protocols.Electroencephalogr Clin Neurophysiol. 1990; 77: 266-275
- Preparation for movement: neural representations of intended direction in three motor areas of the monkey.J Neurophysiol. 1990; 64: 133-150
- Cognitive spatial-motor processes. 3. Motor cortical prediction of movement direction during an instructed delay period.Exp Brain Res. 1989; 75: 183-194
American Psychiatric Association. Obsessive–compulsive and related disorders. In: Diagnostic and Statistical Manual of Mental Disorders, fifth edition. Washington DC: American Psychiatric Publishing; 2013. p. 235–42.
- The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity.J Am Acad Child Adolesc Psychiatry. 1989; 28: 566-573
- Neurophysiology of Tourette syndrome: pathophysiological consideration.Brain Dev. 2003; 25: S62-S69
Nomura Y, Segawa M. Neurology of Tourette's syndrome (TS) TS as a developmental dopamine disorder: a hypothesis Brain Dev 2003;25;S37-42.
- Some characteristics of brain tyrosine hydroxylase.in: Mandell A.J. New concepts in neurotransmitter regulation. Plenum Press, New York-London1973: 53-68
- The selective gating of the N30 cortical component of the somatosensory evoked potentials of median nerve is different in the mesial and dorsolateral frontal cortex: evidence from intracerebral recordings.Clin Neurophysiol. 2003; 114: 981-991
- Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings.Brain. 1991; 114: 2465-2503
- 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.Brain. 1983; 106: 271-311
- Short and middle-latency Median Nerve (MN) SEPSs recorded by depth electrodes in human pre-SMA and SMA-proper.Clin Neurophysiol. 2005; 116: 2664-2674
- Gating of the early components of the frontal and parietal somatosensory evoked potentials in different sensorimotor interference modalities.Electroencephalogr Clin Neurophysiol. 1991; 80: 522-530
- Reduced GABAergic inhibition and abnormal sensory symptoms in children with Tourette syndrome.J Neurophysiol. 2015; 114: 808-817
- Hypofunctioning of sensory gating mechanism in patients with obsessive-compulsive disorder.Biol Psychiatry. 2005; 57: 16-20
- Neurobiology of the premonitory urge in Tourette syndrome: Pathophysiology and treatment implications.J Neuropsychiatry Clin Neurosci. 2017; 29: 95-104
- Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study.Brain. 2006; 129: 2029-2037
- The neural bases of obsessive-compulsive disorder in children and adults.Dev Psychopathol. 2008; 20: 1251-1283
- Role of the sensorimotor cortex in tourette syndrome using multimodal imaging.Hum Brain Mapp. 2014; 35: 5834-5846
- Functional organization of human supplementary motor cortex studied by electrical stimulation.J Neurosci. 1991; 11: 3656-3666
- Repetitive transcranial magnetic stimulation (rTMS) in the treatment of obsessive-compulsive disorder (OCD) and Tourette’s syndrome (TS).Int J Neuropsychopharmacol. 2006; 9: 95-100
- The cortico-basal ganglia integrative network: the role of the thalamus.Brain Res Bull. 2009; 78: 69-74
- Thalamic Local field potentials are related to long-term DBS effects in Tourette syndrome.Front Neurol. 2021; 12578324
- Pallidal and thalamic neural oscillatory patterns in tourette’s syndrome.Ann Neurol. 2018; 84: 505-514
- Premonitory Awareness Facilitates Tic Suppression: Subscales of the Premonitory Urge for Tics Scale and a New Self-Report Questionnaire for Tic-Associated Sensations.Front Psychiatry. 2020; 11: 592
- Premonitory Urge for Tics Scale (PUTS): initial psychometric results and examination of the premonitory urge phenomenon in youths with tic disorders.J Dev Behav Pediatr. 2005; 26: 397-403
Article info
Publication history
Published online: March 04, 2023
Accepted:
February 12,
2023
Received in revised form:
January 29,
2023
Received:
September 8,
2022
Publication stage
In Press Corrected ProofIdentification
Copyright
© 2023 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.
