Reduced GABAergic inhibition and abnormal sensory symptoms in children with Tourette syndrome

Journal of Neurophysiology

Volumn 114, Issue 2, 2015, Pages 808-817

  Puts, Nicolaas A J ^a,b   Harris, Ashley D ^a,b   Crocetti, Deana ^b   Nettles, Carrie ^b   Singer, Harvey S ^a   Tommerdahl, Mark ^c   Edden, Richard A E ^a,b   Mostofsky, Stewart H ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KENNEDY KRIEGER INSTITUTE   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

GABA; Inhibition; Magnetic resonance spectroscopy; Somatosensory function; Tactile processing; Tourette syndrome

Indexed keywords

4 AMINOBUTYRIC ACID;

ARTICLE; ARTIFACT; CHILD; COMORBIDITY; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FREQUENCY DISCRIMINATION; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; GILLES DE LA TOURETTE SYNDROME; HUMAN; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MOTOR CORTEX; NEUROCHEMISTRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; PSYCHOPHYSICS; RESPONSE TIME; RIGHT HEMISPHERE; SCHOOL CHILD; SENSORIMOTOR CORTEX; SENSORY STIMULATION; TACTILE DISCRIMINATION; TACTILE STIMULATION; TOUCH; ADAPTATION; BRAIN CORTEX; METABOLISM; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSICAL STIMULATION; PHYSIOLOGY; REACTION TIME; VIBRATION;

ADAPTATION, PHYSIOLOGICAL; CEREBRAL CORTEX; CHILD; FEMALE; GAMMA-AMINOBUTYRIC ACID; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROPSYCHOLOGICAL TESTS; PHYSICAL STIMULATION; REACTION TIME; SIGNAL DETECTION, PSYCHOLOGICAL; TOUCH PERCEPTION; TOURETTE SYNDROME; VIBRATION;

EID: 84938582395     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00060.2015     Document Type: Article

References (51)

1. Belluscio BA, Jin L, Watters V, Lee TH, Hallett M. Sensory sensitivity to external stimuli in Tourette syndrome patients. Mov Disord 26: 2538–2543, 2011.
2. Blankenburg F, Taskin B, Ruben J, Moosmann M, Ritter P, Curio G, Villringer A. Imperceptible stimuli and sensory processing impediment. Science 299: 1864, 2003.
3. Boy F, Evans CJ, Edden RA, Singh KD, Husain M, Sumner P. Individual differences in subconscious motor control predicted by GABA concentration in SMA. Curr Biol 20: 1779–1785, 2010.
4. Bronfeld M, Yael D, Belelovsky K, Bar-Gad I. Motor tics evoked by striatal disinhibition in the rat. Front Syst Neurosci 7: 50, 2013.
5. Cohen AJ, Leckman JF. Sensory phenomena associated with Gilles de la Tourette’s syndrome. J Clin Psychiatry 53: 319–323, 1992.
6. Du JC, Chiu TF, Lee KM, Wu HL, Yang YC, Hsu SY, Sun CS, Hwang B, Leckman JF. Tourette syndrome in children: an updated review. Pediatr Neonatol 51: 255–264, 2010.
7. Edden RA, Crocetti D, Zhu H, Gilbert DL, Mostofsky SH. Reduced GABA concentration in attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 69: 750–753, 2012.
8. Edden RA, Muthukumaraswamy SD, Freeman TC, Singh KD. Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex. J Neurosci 29: 15721–15726, 2009.
9. Edden RA, Puts NA, Harris AD, Barker PB, Evans CJ. Gannet: a batchprocessing tool for the quantitative analysis of gamma-aminobutyric acidedited MR spectroscopy spectra. J Magn Reson Imaging 40: 1445–1452, 2014.
10. Evans CJ, Puts NA, Robson SE, Boy F, McGonigle DJ, Sumner P, Singh KD, Edden RA. Subtraction artifacts and frequency (mis-)alignment in J-difference GABA editing. J Magn Reson Imaging 38: 970–975, 2013.
11. Favorov OV, Kursun O. Neocortical layer 4 as a pluripotent function linearizer. J Neurophysiol 105: 1342–1360, 2011.
12. Fernandez TV, Sanders SJ, Yurkiewicz IR, Ercan-Sencicek AG, Kim YS, Fishman DO, Raubeson MJ, Song Y, Yasuno K, Ho WS, Bilguvar K, Glessner J, Chu SH, Leckman JF, King RA, Gilbert DL, Heiman GA, Tischfield JA, Hoekstra PJ, Devlin B, Hakonarson H, Mane SM, Gunel M, State MW. Rare copy number variants in Tourette syndrome disrupt genes in histaminergic pathways and overlap with autism. Biol Psychiatry 71: 392–402, 2012.
13. Gao F, Edden RA, Li M, Puts NA, Wang G, Liu C, Zhao B, Wang H, Bai X, Zhao C, Wang X, Barker PB. Edited magnetic resonance spectroscopy detects an age-related decline in brain GABA levels. Neuroimage 78: 75–82, 2013.
14. Harris AD, Glaubitz B, Near J, John Evans C, Puts NA, Schmidt-Wilcke T, Tegenthoff M, Barker PB, Edden RA. Impact of frequency drift on gamma-aminobutyric acid-edited MR spectroscopy. Magn Reson Med 22: 222–223, 2013.
15. Holden JK, Nguyen RH, Francisco EM, Zhang Z, Dennis RG, Tommerdahl M. A novel device for the study of somatosensory information processing. J Neurosci Methods 204: 215–220, 2012.
16. Howells D, Georgiou-Karistianis N, Bradshaw J. The ability to orient attention in Gilles de la Tourette syndrome. Behav Neurol 11: 205–209, 1998.
17. Jankovic J. Tourette syndrome. Phenomenology and classification of tics. Neurol Clin 15: 267–275, 1997.
18. Juliano SL, Whitsel BL, Tommerdahl M, Cheema SS. Determinants of patchy metabolic labeling in the somatosensory cortex of cats: a possible role for intrinsic inhibitory circuitry. J Neurosci 9: 1–12, 1989.
19. Kalanithi PS, Zheng W, Kataoka Y, DiFiglia M, Grantz H, Saper CB, Schwartz ML, Leckman JF, Vaccarino FM. Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc Natl Acad Sci USA 102: 13307–13312, 2005.
20. Karalunas SL, Geurts HM, Konrad K, Bender S, Nigg JT. Annual research review: Reaction time variability in ADHD and autism spectrum disorders: measurement and mechanisms of a proposed trans-diagnostic phenotype. J Child Psychol Psychiatry 55: 685–710, 2014.
21. Kohn A, Whitsel BL. Sensory cortical dynamics. Behav Brain Res 135: 119–126, 2002.
22. Leckman JF, Walker DE, Cohen DJ. Premonitory urges in Tourette’s syndrome. Am J Psychiatry 150: 98–102, 1993.
23. Lerner A, Bagic A, Simmons JM, Mari Z, Bonne O, Xu B, Kazuba D, Herscovitch P, Carson RE, Murphy DL, Drevets WC, Hallett M. Widespread abnormality of the gamma-aminobutyric acid-ergic system in Tourette syndrome. Brain 135: 1926–1936, 2012.
24. Marenco S, Savostyanova AA, van der Veen JW, Geramita M, Stern A, Barnett AS, Kolachana B, Radulescu E, Zhang F, Callicott JH, Straub RE, Shen J, Weinberger DR. Genetic modulation of GABA levels in the anterior cingulate cortex by GAD1 and COMT. Neuropsychopharmacology 35: 1708–1717, 2010.
25. McCairn KW, Iriki A, Isoda M. Global dysrhythmia of cerebro-basal ganglia-cerebellar networks underlies motor tics following striatal disinhibition. J Neurosci 33: 697–708, 2013.
26. McLaughlin DF, Juliano SL. Disruption of layer 4 development alters laminar processing in ferret somatosensory cortex. Cereb Cortex 15: 1791–1803, 2005.
27. Mescher M, Merkle H, Kirsch J, Garwood M, Gruetter R. Simultaneous in vivo spectral editing and water suppression. NMR Biomed 11: 266–272, 1998.
28. Miguel EC, do Rosario-Campos MC, Prado HS, do Valle R, Rauch SL, Coffey BJ, Baer L, Savage CR, O’Sullivan RL, Jenike MA, Leckman JF. Sensory phenomena in obsessive-compulsive disorder and Tourette’s disorder. J Clin Psychiatry 61: 150–157, 2000.
29. Mullins PG, McGonigle DJ, O’Gorman RL, Puts NA, Vidyasagar R, Evans CJ, Cardiff Symposium on MRS of GABA, Edden RA. Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. Neuroimage 86: 43–52, 2014.
30. Near J, Edden R, Evans CJ, Paquin R, Harris A, Jezzard P. Frequency and phase drift correction of magnetic resonance spectroscopy data by spectral registration in the time domain. Magn Reson Med (January 16, 2014). doi:10.1002/mrm.25094.
31. O’Gorman RL, Michels L, Edden RA, Murdoch JB, Martin E. In vivo detection of GABA and glutamate with MEGA-PRESS: reproducibility and gender effects. J Magn Reson Imaging 33: 1262–1267, 2011.
32. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97–113, 1971.
33. Puts NA, Edden RA. In vivo magnetic resonance spectroscopy of GABA: a methodological review. Prog Nucl Magn Reson Spectrosc 60: 29–41, 2012.
34. Puts NA, Edden RA, Evans CJ, McGlone F, McGonigle DJ. Regionally specific human GABA concentration correlates with tactile discrimination thresholds. J Neurosci 31: 16556–16560, 2011.
35. Puts NA, Edden RA, Wodka EL, Mostofsky SH, Tommerdahl M. A vibrotactile behavioral battery for investigating somatosensory processing in children and adults. J Neurosci Methods 218: 39–47, 2013.
36. Puts NA, Wodka EL, Tommerdahl M, Mostofsky SH, Edden RA. Impaired tactile processing in children with autism spectrum disorder. J Neurophysiol 111: 1803–1811, 2014.
37. Reich W. Diagnostic interview for children and adolescents (DICA). J Am Acad Child Adolesc Psychiatry 39: 59–66, 2000.
38. Robertson MM, Trimble MR, Lees AJ. The psychopathology of the Gilles de la Tourette syndrome. A phenomenological analysis. Br J Psychiatry 152: 383–390, 1988.
39. Seamans JK, Gorelova N, Durstewitz D, Yang CR. Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21: 3628–3638, 2001.
40. Swadlow HA. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13: 25–32, 2003.
41. Tannan V, Holden JK, Zhang Z, Baranek GT, Tommerdahl MA. Perceptual metrics of individuals with autism provide evidence for disinhibition. Autism Res 1: 223–230, 2008.
42. Tannan V, Simons S, Dennis RG, Tommerdahl M. Effects of adaptation on the capacity to differentiate simultaneously delivered dual-site vibrotactile stimuli. Brain Res 1186: 164–170, 2007.
43. Tannan V, Whitsel BL, Tommerdahl MA. Vibrotactile adaptation enhances spatial localization. Brain Res 1102: 109–116, 2006.
44. Tian Y, Gunther JR, Liao IH, Liu D, Ander BP, Stamova BS, Lit L, Jickling GC, Xu H, Zhan X, Sharp FR. GABA- and acetylcholine-related gene expression in blood correlate with tic severity and microarray evidence for alternative splicing in Tourette syndrome: a pilot study. Brain Res 1381: 228–236, 2011.
45. Wang S, Qi F, Li J, Zhao L, Li A. Effects of Chinese herbal medicine Ningdong granule on regulating dopamine (DA)/serotonin (5-TH) and gamma-amino butyric acid (GABA) in patients with Tourette syndrome. Biosci Trends 6: 212–218, 2012.
46. Wechsler D. Wechsler Intelligence Scale for Children. San Antonio, TX: The Psychological Corporation, 2003.
47. Whitsel BL, Favorov O, Tommerdahl M, Diamond M, Juliano SJ, Kelly D. Dynamic processes govern the somatosensory cortical response to natural stimulation. In: Sensory Processing in the Mammalian Brain: Neural Substrates and Experimental Strategies. New York: Oxford Univ. Press, 1989, p. 84–116.
48. Whitsel BL, Kelly EF, Quibrera M, Tommerdahl M, Li Y, Favorov OV, Xu M, Metz CB. Time-dependence of SI RA neuron response to cutaneous flutter stimulation. Somatosens Motor Res 20: 45–69, 2003.
49. Woods DW, Piacentini JC, Scahill L, Peterson AL, Wilhelm S, Chang S, Deckersbach T, McGuire J, Specht M, Conelea CA, Rozenman M, Dzuria J, Liu H, Levi-Pearl S, Walkup JT. Behavior therapy for tics in children: acute and long-term effects on psychiatric and psychosocial functioning. J Child Neurol 26: 858–865, 2011.
50. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P. Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120: 141–157, 1997.
51. Zhang Z, Francisco EM, Holden JK, Dennis RG, Tommerdahl M. Somatosensory information processing in the aging population. Front Aging Neurosci 3: 18, 2011.