Auditory event-related potentials demonstrate early cognitive impairment in children with subclinical hypothyroidism
-
Sibel Kocaaslan Atli
,
Nihal Olgaç Dündar
Abstract
Background
The aim of this study was to examine the cognitive functions of children with subclinical hypothyroidism (SH) and healthy children with the use of auditory event-related potentials (AERPs) and neuropsychological tests.
Methods
Twenty children aged between 8 and 17 years, diagnosed with SH, and 20 age-matched healthy controls were included in this study. A classical auditory oddball paradigm was applied during the electroencephalography (EEG) recordings, and event-related potentials (ERPs) were evaluated between the 0.5- and 20-Hz frequency intervals. P1, N1, P2, N2 and P3 amplitudes and latencies were measured in Fz, FCz, Cz, CPz, Pz and Oz electrodes. Additionally, a number of neuropsychological tests evaluating the reaction time and various cognitive functions were carried out.
Results
In children with SH, P3 amplitudes in FCz, Cz and CPz electrodes were significantly lower than those in controls (p < 0.05). In addition to this, the P1N1 and N1P2 peak-to-peak amplitude values were also found to be smaller for children with SH than controls (p < 0.05). With regard to the neuropsychological tests, no significant difference was observed between the SH and control groups on any of the cognitive test parameters, reaction time or correct response rates.
Conclusions
In the present study, while children with SH did not differ from controls with respect to their cognitive functions evaluated via neuropsychological tests, cognitive differences were detected via electrophysiological investigations. This result implies that implicit changes in cognition which are not yet overtly reflected on neuropsychological tests may be detected at an early stage in children with SH.
Acknowledgments
This work was supported by IKCU BAP-Project 2013-3-TSBP-12.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Samuels MH. Cognitive function in subclinical hypothyroidism. J Clin Endocrinol Metab 2010;95:3611–3.10.1210/jc.2010-1242Search in Google Scholar PubMed
2. Kim JM, Stewart R, Kim SY, Bae KY, Yang SJ, et al. Thyroid stimulating hormone, cognitive impairment and depression in an older Korean population. Psychiatry Investig 2010;7:264–9.10.4306/pi.2010.7.4.264Search in Google Scholar PubMed PubMed Central
3. Davis JD, Tremont G. Neuropsychiatric aspects of hypothyroidism and treatment reversibility. Minerva Endocrinol 2007;32:49–65.Search in Google Scholar
4. Aijaz NJ, Flaherty EM, Preston T, Bracken SS, Lane AH, et al. Neurocognitive function in children with compensated hypothyroidism: lack of short term effects on or off thyroxin. BMC Endocr Disord 2006;6:2.10.1186/1472-6823-6-2Search in Google Scholar PubMed PubMed Central
5. Gan EH, Pearce SH. The thyroid in mind: cognitive function and low thyrotropin in older people. J Clin Endocrinol Metab 2012;97:3438–49.10.1210/jc.2012-2284Search in Google Scholar PubMed PubMed Central
6. Samuels MH, Schuff KG, Carlson NE, Carello P, Janowsky JS. Health status, mood and cognition in experimentally induced subclinical hypothyroidism. J Clin Endocrinol Metab 2007;92:2545–51.10.1210/jc.2007-0011Search in Google Scholar PubMed
7. Zhu DF, Wang ZX, Zhang DR, Pan ZL, He S, et al. fMRI revealed neural substrate for reversible working memory dysfunction in subclinical hypothyroidism. Brain 2006;129:2923–30.10.1093/brain/awl215Search in Google Scholar PubMed
8. Wijsman LW, de Craen AJ, Trompet S, Gussekloo J, Stott DJ, et al. Subclinical thyroid dysfunction and cognitive decline in old age. PLoS One 2013;8:e59199.10.1371/journal.pone.0059199Search in Google Scholar PubMed PubMed Central
9. Roberts LM, Pattison H, Roalfe A, Franklyn J, Wilson S, et al. Is subclinical thyroid dysfunction in the elderly associated with depression or cognitive dysfunction? Ann Intern Med 2006;145:573–81.10.7326/0003-4819-145-8-200610170-00006Search in Google Scholar PubMed
10. St John JA, Henderson VW, Gatto NM, McCleary CA, Spencer CA, et al. Mildly elevated TSH and cognition in middle-aged and older adults. Thyroid 2009;19:111–7.10.1089/thy.2008.0226Search in Google Scholar PubMed PubMed Central
11. Ergür AT, Taner Y, Ata E, Melek E, Erdoğan Bakar E, et al. Neurocognitive functions in children and adolescents with subclinical hypothyroidism. J Clin Res Pediatr Endocrinol 2012;4:21–4.10.4274/Jcrpe.497Search in Google Scholar PubMed PubMed Central
12. Sangün Ö, Demirci S, Dündar N, Pirgon Ö, Koca T, et al. The effects of six-month l-thyroxine treatment on cognitive functions and event-related brain potentials in children with subclinical hypothyroidism. J Clin Res Pediatr Endocrinol 2015;7:102–8.10.4274/jcrpe.1684Search in Google Scholar
13. Catli G, Abacı A, Büyükgebiz A, Bober E. Subclinical hypothyroidism in children and adolescence. J Pediatr Endocrinol Metab 2014;27:1049–57.Search in Google Scholar
14. Başar E, Başar-Eroğlu C, Demiralp T, Schürmann M. The compound P300–40 Hz response of the human brain. Electroencephalogr Clin Neurophysiol 1993;87:14.Search in Google Scholar
15. Polich J. Attention, probability, and task demands as determinants of P300 latency from auditory stimuli. Electroencephalogr Clin Neurophysiol 1986;63:251–9.10.1016/0013-4694(86)90093-3Search in Google Scholar
16. Başar E, editor. EEG-Brain dynamics. Relation between EEG and brain evoked potentials. Amsterdam, The Netherlands: Elseiver-North Holland Biomedical Press, 1980.Search in Google Scholar
17. Nunez P, editor. Electric fields of the brain: the neurophysics of EEG. New York: Oxford University Press, 2006.10.1093/acprof:oso/9780195050387.001.0001Search in Google Scholar
18. Picton TW, Bentin S, Berg P, Donchin E, Hillyard SA, et al. Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. Psychophysiology 2000;37:127–52.10.1111/1469-8986.3720127Search in Google Scholar
19. Plourde G. Auditory evoked potentials. Best Pract Res Clin Anaesthesiol 2006;20:129–39.10.1016/j.bpa.2005.07.012Search in Google Scholar
20. Çatli G, Kir M, Anik A, Yilmaz N, Böber E, et al. The effect of L-thyroxine treatment on left ventricular functions in children with subclinical hypothyroidism. Arch Dis Child 2015;100:130–7.10.1136/archdischild-2014-306381Search in Google Scholar
21. The PEBL Psychological test battery. Available at: http://pebl.sourceforge.net/battery.html; Accessed: 12 December 2014.Search in Google Scholar
22. Wilkinson RT, Houghton D. Field test of arousal: a portable reaction timer with data storage. Hum Factors 1982;24:487–93.10.1177/001872088202400409Search in Google Scholar
23. Conners CK, Epstein JN, Angold A, Klaric J. Continuous performance test performance in a normative epidemiological sample. J Abnorm Child Psychol 2003;31:555–62.10.1023/A:1025457300409Search in Google Scholar
24. Simon JR. Reactions toward the source of stimulation. J Exp Psychol 1969;81:174–6.10.1037/h0027448Search in Google Scholar
25. Savasir I, Sahin N, editors. Wechsler intelligence scale for children-revised (WISC-R) Turkish handbook. Ankara: Turkish Psychological Association Publications, 1995.Search in Google Scholar
26. Johnson Jr R, Donchin E. On how P300 amplitude varies with the utility of the eliciting stimuli. Electroencephalogr Clin Neurophysiol 1978;44:424–37.10.1016/0013-4694(78)90027-5Search in Google Scholar
27. Başar-Eroğlu C, Başar E. A compound P300–40 Hz response of the cat hippocampus. Int J Neurosci 1991;60:227–37.10.3109/00207459109167035Search in Google Scholar PubMed
28. Goodin DS. Cognitive event-related potentials. J Clin Neurophysiol 1998;15:2.10.1097/00004691-199801000-00002Search in Google Scholar PubMed
29. Azizian A, Polich J. Evidence for attentional gradient in the serial position memory curve from event-related potentials. J Cogn Neurosci 2007;19:2071–81.10.1162/jocn.2007.19.12.2071Search in Google Scholar PubMed PubMed Central
30. Wang S, Yang C, Liu Y, Shao Z, Jackson T. Early and late stage processing abnormalities in autism spectrum disorders: an ERP study. PLoS One 2017;12:e0178542. 10.1371/journal.pone.0178542Search in Google Scholar PubMed PubMed Central
31. Sur S, Sinha VK. Event-related potential: an overview. Ind Psychiatry J 2009;18:70–3.10.4103/0972-6748.57865Search in Google Scholar PubMed PubMed Central
32. Polich J. Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 2007;118:2128–48.10.1016/j.clinph.2007.04.019Search in Google Scholar PubMed PubMed Central
33. Yener GG, Başar E. Sensory evoked and event related oscillations in Alzheimer’s disease: a short review. Cogn Neurodyn 2010;4:263–74.10.1007/s11571-010-9138-5Search in Google Scholar PubMed PubMed Central
34. Frodl T, Hampel H, Juckel G, Bürger K, Padberg F, et al. Value of event-related P300 subcomponents in the clinical diagnosis of mild cognitive impairment and Alzheimer’s disease. Psychophysiology 2002;39:V175–81.10.1111/1469-8986.3920175Search in Google Scholar
35. Pedroso RV, Fraga FJ, Corazza DI, Andreatto CA, Coelho FG, et al. P300 latency and amplitude in Alzheimer’s disease: a systematic review. Braz J Otorhinolaryngol 2012;78:126–32.10.1590/S1808-86942012000400023Search in Google Scholar
36. Emek Savaş DD, Çavuşoğlu B, Hünerli D, Yerlikaya D, Gökçeoğlu A, et al. P300 responses are associated with subcortical gray matter volume in amnestic mild cognitive impairment and normal aging. Int J of Psychophysiol 2016;108(Suppl):S304.10.1016/j.ijpsycho.2016.07.306Search in Google Scholar
37. Özmüş G, Yerlikaya D, Gökçeoğlu A, Emek Savaş DD, Çakmur R, et al. Demonstration of early cognitive impairment in Parkinson’s disease with visual P300 responses. Noro Psikiyatr Ars 2017;54:21–7.10.5152/npa.2016.12455Search in Google Scholar PubMed PubMed Central
38. Khedr EM, El Toony LF, Tarkhan MN, Abdella G. Peripheral and central nervous system alterations in hypothyroidism: electrophysiological findings. Neuropsychobiol 2000;41:88–94.10.1159/000026638Search in Google Scholar PubMed
39. Tütüncü NB, Karataş M, Sözay S. Prolonged P300 latency in thyroid failure: a paradox. P300 latency recovers later in mild hypothyroidism than in severe hypothyroidism. Thyroid 2004;14:622–7.10.1089/1050725041692837Search in Google Scholar PubMed
40. Dejanović M, Ivetić V, Nestorović V, Milanović Z, Erić M. The value of P300 event related potentials in the assessment of cognitive function in subclinicalhypothyroidism. Minerva Endocrinol 2017;42:15–23.10.23736/S0391-1977.16.02327-0Search in Google Scholar PubMed
41. Paladugu S, Hanmayyagari BR, Kudugunti N, Reddy R, Sahay R, et al. Improvement in subclinical cognitive dysfunction with thyroxine therapy in hypothyroidism: a study from tertiary care center. Indian J Endocr Metab 2015;19:829–33.10.4103/2230-8210.167547Search in Google Scholar PubMed PubMed Central
42. Jensovsky J, Ruzicka E, Spackova N, Hejdukova B. Changes of event related potential and cognitive processes in patients with Subclinical hypothyroidism after thyroxine treatment. Endocr Regul 2002;36:115–22.Search in Google Scholar
43. Näätänen R, Picton T. The N1 wave of the human alectric and magnetic response to aound: a review and an analysis of the component structure. Psychophysiology 1987;24:375–425.10.1111/j.1469-8986.1987.tb00311.xSearch in Google Scholar PubMed
44. Lijffijt M, Lane SD, Meier SL, Boutros NN, Burrough S, et al. P50, N100, and P200 sensory gating: relationships with behavioral inhibition, attention, and working memory. Psychophysiology 2009;46:1059.10.1111/j.1469-8986.2009.00845.xSearch in Google Scholar PubMed PubMed Central
45. Boutros NN, Korzyukov O, Jansen B, Feingold A, Bella M. Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res 2004;126:203–15.10.1016/j.psychres.2004.01.007Search in Google Scholar PubMed
46. Oken BS, Salinsky MC, Elsas SM. Vigilance, alertness or sustained attention: physiological basis and measurement. Clin Neurophysiol 2006;17:1885–901.10.1016/j.clinph.2006.01.017Search in Google Scholar PubMed PubMed Central
47. Loh S, Lamond N, Dorrian J, Roach G, Dawson D. The Validity of psychomotor vigilance tasks of less than 10 minute duration. Behav Res Methods Instrum Comput 2004;36:334–9.10.3758/BF03195580Search in Google Scholar PubMed
48. Smallwood JD, Davies JB, Heim D, Finnigan F, Sudberry M, et al. Subjective experience and the attentional lapse: task engagement and disengagement during sustained attention. Conscious Cogn 2004;13:657–90.10.1016/j.concog.2004.06.003Search in Google Scholar PubMed
49. Hancock PA, Vasmatzidis I. Human occupational and performance limits under stress the thermal environment as a prototypical example. Ergonomics 1998;41:1169–91.10.1080/001401398186469Search in Google Scholar PubMed
50. Welford AT. Reaction time, speed of performance, and age. Ann N Y Acad Sci 1988;515:1–17.10.1111/j.1749-6632.1988.tb32958.xSearch in Google Scholar PubMed
©2019 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Review
- Effect of safflower yellow on early type II diabetic nephropathy: a systematic review and meta-analysis of randomized controlled trials
- Original Articles
- Genomic study via chromosomal microarray analysis in a group of Romanian patients with obesity and developmental disability/intellectual disability
- Clinical and molecular characteristics and time of diagnosis of patients with classical galactosemia in an unscreened population in Turkey
- Assessment of retinal thickness as a marker of brain masculinization in children with congenital adrenal hyperplasia: a pilot study
- Auditory event-related potentials demonstrate early cognitive impairment in children with subclinical hypothyroidism
- Cardiovascular risk factors in children with type 1 diabetes mellitus
- The relationship between serum FGF-23 concentration and insulin resistance, prediabetes and dyslipidemia in obese children and adolescents
- The metabolic consequences of overweight in a cohort of children with type 1 diabetes
- The spectrum of pediatric adrenal insufficiency: insights from 34 years of experience
- Growth screening in children aged 3–5 years: a useful tool for public health programs in community pediatrics
- Selective receptor-mediated impairment of growth factor activity in neonatal- and X-linked adrenoleukodystrophy patients
- Determinants for low bone mineral density in pre-school children: a matched case-control study in Wuhan, China
- Genetic polymorphisms associated with obesity and non-alcoholic fatty liver disease in Asian Indian adolescents
- Maturity onset diabetes of the young (MODY) in Chinese children: genes and clinical phenotypes
- Severe, persistent neonatal hypoglycemia as a presenting feature in patients with congenital hypopituitarism: a review of our case series
- Case Reports
- Short stature in a boy with atypical progeria syndrome due to LMNA c.433G>A [p.(Glu145Lys)]: apparent growth hormone deficiency but poor response to growth hormone therapy
- A novel mutation leading to the lethal form of carnitine palmitoyltransferase type-2 deficiency
- Diagnosis of cyclic Cushing’s disease manifests as early morning hyperglycemia in a patient with previously well-controlled type 1 diabetes
- Short Communication
- Replacement of breastfeeding with medical food for the treatment of galactosemia and phenylketonuria: maternal stress
Articles in the same Issue
- Frontmatter
- Review
- Effect of safflower yellow on early type II diabetic nephropathy: a systematic review and meta-analysis of randomized controlled trials
- Original Articles
- Genomic study via chromosomal microarray analysis in a group of Romanian patients with obesity and developmental disability/intellectual disability
- Clinical and molecular characteristics and time of diagnosis of patients with classical galactosemia in an unscreened population in Turkey
- Assessment of retinal thickness as a marker of brain masculinization in children with congenital adrenal hyperplasia: a pilot study
- Auditory event-related potentials demonstrate early cognitive impairment in children with subclinical hypothyroidism
- Cardiovascular risk factors in children with type 1 diabetes mellitus
- The relationship between serum FGF-23 concentration and insulin resistance, prediabetes and dyslipidemia in obese children and adolescents
- The metabolic consequences of overweight in a cohort of children with type 1 diabetes
- The spectrum of pediatric adrenal insufficiency: insights from 34 years of experience
- Growth screening in children aged 3–5 years: a useful tool for public health programs in community pediatrics
- Selective receptor-mediated impairment of growth factor activity in neonatal- and X-linked adrenoleukodystrophy patients
- Determinants for low bone mineral density in pre-school children: a matched case-control study in Wuhan, China
- Genetic polymorphisms associated with obesity and non-alcoholic fatty liver disease in Asian Indian adolescents
- Maturity onset diabetes of the young (MODY) in Chinese children: genes and clinical phenotypes
- Severe, persistent neonatal hypoglycemia as a presenting feature in patients with congenital hypopituitarism: a review of our case series
- Case Reports
- Short stature in a boy with atypical progeria syndrome due to LMNA c.433G>A [p.(Glu145Lys)]: apparent growth hormone deficiency but poor response to growth hormone therapy
- A novel mutation leading to the lethal form of carnitine palmitoyltransferase type-2 deficiency
- Diagnosis of cyclic Cushing’s disease manifests as early morning hyperglycemia in a patient with previously well-controlled type 1 diabetes
- Short Communication
- Replacement of breastfeeding with medical food for the treatment of galactosemia and phenylketonuria: maternal stress
