Korean Journal of Biological Psychiatry (생물정신의학)

The Korean Society of Biological Psychiatry (대한생물정신의학회)
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Effects of Korean Red Ginseng on White Matter Microstructure and Cognitive Functions : A Focus on Intrusion Errors

고려 홍삼이 대뇌 백질 미세구조 및 인지기능에 미치는 효과 : 침입 오류를 중심으로

  • 정현석 (가톨릭대학교 인천성모병원 영상의학과) ;
  • 김영훈 (이화여자대학교 뇌융합과학연구원) ;
  • 이선호 (이화여자대학교 뇌융합과학연구원) ;
  • 염아림 (이화여자대학교 뇌융합과학연구원) ;
  • 강일향 (이화여자대학교 뇌융합과학연구원) ;
  • 김지은 (이화여자대학교 뇌융합과학연구원) ;
  • 이정현 (이화여자대학교 뇌융합과학연구원) ;
  • 반순현 (이화여자대학교 뇌융합과학연구원) ;
  • 임수미 (이화여자대학교 뇌융합과학연구원) ;
  • 이선혜 (이화여자대학교 뇌융합과학연구원)
  • Received : 2015.01.19
  • Accepted : 2015.05.06
  • Published : 2015.05.31
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Abstract

Objectives Although ginseng has been reported to protect neuronal cells and improve various cognitive functions, relationship between ginseng supplementation and response inhibition, one of the important cognitive domains has not been explored. In addition, effects of ginseng on in vivo human brain have not been investigated using the diffusion tensor imaging (DTI). The purpose of the current study is to investigate changes in intrusion errors and white matter microstructure after Korean Red Ginseng supplementation using standardized neuropsychological tests and DTI. Methods Fifty-one healthy participants were randomly allocated to the Korean Red Ginseng (n = 26) or placebo (n = 25) groups for 8 weeks. The California Verbal Learning Test was used to assess the number of intrusion errors. Intelligence quotient (IQ) was measured with the Korean Wechsler Adult Intelligence Scale. Depressive and anxiety symptoms were evaluated using Hamilton Depression Rating Scale, Hamilton Anxiety Rating Scale, and Hopkins Symptom Checklist-25. The fractional anisotropy (FA) was measured from the brain DTI data. Results After the 8-week intervention, Korean Red Ginseng supplementation significantly reduced intrusion errors after adjusting age, sex, IQ, and baseline score of the intrusion errors (p for interaction = 0.005). Change in FA values in the left anterior corona radiata was greater in the Korean Red Ginseng group compared to the placebo group (t = 4.29, p = 0.04). Conclusions Korean Red Ginseng supplementation may be efficacious for improving response inhibition and white matter microstructure integrity in the prefrontal cortex.

Keywords

References

  1. Huang KC. The Pharmacology of Chinese Herbs. Boca Raton, FL: CRC Press;1998.
  2. Liu YW, Zhu X, Li W, Lu Q, Wang JY, Wei YQ, et al. Ginsenoside Re attenuates diabetes-associated cognitive deficits in rats. Pharmacol Biochem Behav 2012;101:93-98. https://doi.org/10.1016/j.pbb.2011.12.003
  3. Ye R, Kong X, Yang Q, Zhang Y, Han J, Li P, et al. Ginsenoside Rd in experimental stroke: superior neuroprotective efficacy with a wide therapeutic window. Neurotherapeutics 2011;8:515-525. https://doi.org/10.1007/s13311-011-0051-3
  4. Sorensen H, Sonne J. A double-masked study of the effects of ginseng on cognitive functions. Curr Ther Res 1996;57:959-968. https://doi.org/10.1016/S0011-393X(96)80114-7
  5. Sunram-Lea SI, Birchall RJ, Wesnes KA, Petrini O. The effect of acute administration of 400 mg of Panax ginseng on cognitive performance and mood in healthy young volunteers. Curr Top Nutraceutical Res 2005;3:65-74.
  6. D'Angelo L, Grimaldi R, Caravaggi M, Marcoli M, Perucca E, Lecchini S, et al. A double-blind, placebo-controlled clinical study on the effect of a standardized ginseng extract on psychomotor performance in healthy volunteers. J Ethnopharmacol 1986;16:15-22. https://doi.org/10.1016/0378-8741(86)90063-2
  7. Kennedy DO, Scholey AB, Wesnes KA. Dose dependent changes in cognitive performance and mood following acute administration of Ginseng to healthy young volunteers. Nutr Neurosci 2001;4:295-310. https://doi.org/10.1080/1028415X.2001.11747370
  8. Kennedy DO, Reay JL, Scholey AB. Effects of 8 weeks administration of Korean Panax ginseng extract on the mood and cognitive performance of healthy individuals. J Ginseng Res 2007;37:34-43.
  9. Lee ST, Chu K, Sim JY, Heo JH, Kim M. Panax ginseng enhances cognitive performance in Alzheimer disease. Alzheimer Dis Assoc Disord 2008;22:222-226. https://doi.org/10.1097/WAD.0b013e31816c92e6
  10. Heo JH, Lee ST, Chu K, Oh MJ, Park HJ, Shim JY, et al. An open-label trial of Korean red ginseng as an adjuvant treatment for cognitive impairment in patients with Alzheimer's disease. Eur J Neurol 2008;15:865-868. https://doi.org/10.1111/j.1468-1331.2008.02157.x
  11. Mostofsky SH, Simmonds DJ. Response inhibition and response selection: two sides of the same coin. J Cogn Neurosci 2008;20:751-761. https://doi.org/10.1162/jocn.2008.20500
  12. Chambers CD, Garavan H, Bellgrove MA. Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neurosci Biobehav Rev 2009;33:631-646. https://doi.org/10.1016/j.neubiorev.2008.08.016
  13. Bjorklund DF, Harnishfeger KK. The resources construct in cognitive development: Diverse sources of evidence and a theory of inefficient inhibition. Dev Rev 1990;10:48-71. https://doi.org/10.1016/0273-2297(90)90004-N
  14. Luna B, Sweeney JA. The emergence of collaborative brain function: fMRI studies of the development of response inhibition. Ann N Y Acad Sci 2004;1021:296-309. https://doi.org/10.1196/annals.1308.035
  15. Oosterlaan J, Logan GD, Sergeant JA. Response inhibition in AD/HD, CD, comorbid AD/HD + CD, anxious, and control children: a meta-analysis of studies with the stop task. J Child Psychol Psychiatry 1998;39:411-425. https://doi.org/10.1017/S0021963097002072
  16. Challman TD, Lipsky JJ. Methylphenidate: its pharmacology and uses. Mayo Clin Proc 2000;75:711-721. https://doi.org/10.1016/S0025-6196(11)64618-1
  17. Aron AR, Dowson JH, Sahakian BJ, Robbins TW. Methylphenidate improves response inhibition in adults with attention-deficit/hyperactivity disorder. Biol Psychiatry 2003;54:1465-1468. https://doi.org/10.1016/S0006-3223(03)00609-7
  18. Chamberlain SR, Hampshire A, Muller U, Rubia K, Del Campo N, Craig K, et al. Atomoxetine modulates right inferior frontal activation during inhibitory control: a pharmacological functional magnetic resonance imaging study. Biol Psychiatry 2009;65:550-555. https://doi.org/10.1016/j.biopsych.2008.10.014
  19. Lee SC, Lee SJ, Chung KS, You KH, Kim HS. The central effects of red ginseng total saponin component. Korean J Ginseng Sci 1995;19:22-26.
  20. Niederhofer H. Panax ginseng may improve some symptoms of attention-deficit hyperactivity disorder. J Diet Suppl 2009;6:22-27. https://doi.org/10.1080/19390210802687221
  21. Heatherton TF, Wagner DD. Cognitive neuroscience of self-regulation failure. Trends Cogn Sci 2011;15:132-139. https://doi.org/10.1016/j.tics.2010.12.005
  22. Swick D, Ashley V, Turken U. Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. Neuroimage 2011;56:1655-1665. https://doi.org/10.1016/j.neuroimage.2011.02.070
  23. Diler RS, Pan LA, Segreti A, Ladouceur CD, Forbes E, Cela SR, et al. Differential anterior cingulate activity during response inhibition in depressed adolescents with bipolar and unipolar major depressive disorder. J Can Acad Child Adolesc Psychiatry 2014;23:10-19.
  24. King AV, Linke J, Gass A, Hennerici MG, Tost H, Poupon C, et al. Microstructure of a three-way anatomical network predicts individual differences in response inhibition: a tractography study. Neuroimage 2012;59:1949-1959. https://doi.org/10.1016/j.neuroimage.2011.09.008
  25. Wozniak JR, Lim KO. Advances in white matter imaging: a review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging. Neurosci Biobehav Rev 2006; 30:762-774. https://doi.org/10.1016/j.neubiorev.2006.06.003
  26. Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry 1960;23:56-62. https://doi.org/10.1136/jnnp.23.1.56
  27. Hamilton M. The assessment of anxiety states by rating. Br J Med Psychol 1959;32:50-55. https://doi.org/10.1111/j.2044-8341.1959.tb00467.x
  28. Mollica RF. Measuring trauma, measuring torture: instructions and guidance on the utilization of the Harvard Program in Refugee Trauma's versions of The Hopkins Symptom Checklist-25 (HSCL-25) & The Harvard Trauma Questionnaire (HTQ). Harvard Program in Refugee Trauma;2004.
  29. Delis DC, Kramer JH, Kaplan E, Ober BA. The California Verbal Learning Test. San Antonio, TX: Psychological Corporation;1987.
  30. Mahone EM, Koth CW, Cutting L, Singer HS, Denckla MB. Executive function in fluency and recall measures among children with Tourette syndrome or ADHD. J Int Neuropsychol Soc 2001;7:102-111. https://doi.org/10.1017/S1355617701711101
  31. Hernandez MT, Sauerwein HC, Jambaque I, de Guise E, Lussier F, Lortie A, et al. Attention, memory, and behavioral adjustment in children with frontal lobe epilepsy. Epilepsy Behav 2003;4:522-536. https://doi.org/10.1016/j.yebeh.2003.07.014
  32. Paolo AM, Troster AI, Ryan JJ. Test-retest stability of the California verbal learning test in older persons. Neuropsychology 1997;11:613-616. https://doi.org/10.1037/0894-4105.11.4.613
  33. Yeom T, Park Y, Oh K, Kim J, Lee Y. K-Wechsler Adult Intelligence Scale. Seoul: Korea Guidance;1992.
  34. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-1505. https://doi.org/10.1016/j.neuroimage.2006.02.024
  35. Pattyn N, Neyt X, Henderickx D, Soetens E. Psychophysiological investigation of vigilance decrement: boredom or cognitive fatigue? Physiol Behav 2008;93:369-378. https://doi.org/10.1016/j.physbeh.2007.09.016
  36. Damrad-Frye R, Laird JD. The experience of boredom: The role of the self-perception of attention. J Pers Soc Psychol 1989;57:315-320. https://doi.org/10.1037/0022-3514.57.2.315
  37. Seghete KL, Herting MM, Nagel BJ. White matter microstructure correlates of inhibition and task-switching in adolescents. Brain Res 2013;1527:15-28. https://doi.org/10.1016/j.brainres.2013.06.003
  38. Mori S, Wakana S, Nagae-Poetscher LM, van Zijl PC. MRI atlas of human white matter. Amsterdam: Elsevier;2005.
  39. Posner MI, Petersen SE. The attention system of the human brain. Annu Rev Neurosci 1990;13:25-42. https://doi.org/10.1146/annurev.ne.13.030190.000325
  40. Niogi S, Mukherjee P, Ghajar J, McCandliss BD. Individual differences in distinct components of attention are linked to anatomical variations in distinct white matter tracts. Front Neuroanat 2010;4:2.
  41. Niogi SN, Mukherjee P, Ghajar J, Johnson CE, Kolster R, Lee H, et al. Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain 2008;131(Pt 12): 3209-3221. https://doi.org/10.1093/brain/awn247
  42. Tang YY, Lu Q, Geng X, Stein EA, Yang Y, Posner MI. Short-term meditation induces white matter changes in the anterior cingulate. Proc Natl Acad Sci U S A 2010;107:15649-15652. https://doi.org/10.1073/pnas.1011043107
  43. van Ewijk H, Heslenfeld DJ, Zwiers MP, Buitelaar JK, Oosterlaan J. Diffusion tensor imaging in attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Neurosci Biobehav Rev 2012; 36:1093-1106. https://doi.org/10.1016/j.neubiorev.2012.01.003
  44. Pavuluri MN, Yang S, Kamineni K, Passarotti AM, Srinivasan G, Harral EM, et al. Diffusion tensor imaging study of white matter fiber tracts in pediatric bipolar disorder and attention-deficit/hyperactivity disorder. Biol Psychiatry 2009;65:586-593. https://doi.org/10.1016/j.biopsych.2008.10.015
  45. Takeuchi H, Sekiguchi A, Taki Y, Yokoyama S, Yomogida Y, Komuro N, et al. Training of working memory impacts structural connectivity. J Neurosci 2010;30:3297-3303. https://doi.org/10.1523/JNEUROSCI.4611-09.2010
  46. Serrien DJ, Ivry RB, Swinnen SP. Dynamics of hemispheric specialization and integration in the context of motor control. Nat Rev Neurosci 2006;7:160-166.
  47. Serrien DJ, Sovijarvi-Spape MM. Cognitive control of response inhibition and switching: hemispheric lateralization and hand preference. Brain Cogn 2013;82:283-290. https://doi.org/10.1016/j.bandc.2013.04.013
  48. Swick D, Ashley V, Turken AU. Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci 2008;9:102. https://doi.org/10.1186/1471-2202-9-102
  49. Garavan H, Ross TJ, Stein EA. Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc Natl Acad Sci U S A 1999;96:8301-8306. https://doi.org/10.1073/pnas.96.14.8301
  50. Konishi S, Nakajima K, Uchida I, Sekihara K, Miyashita Y. No-go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging. Eur J Neurosci 1998;10: 1209-1213. https://doi.org/10.1046/j.1460-9568.1998.00167.x
  51. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW. Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 2003;6:115-116. https://doi.org/10.1038/nn1003
  52. Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF. Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 2005;57:1336-1346. https://doi.org/10.1016/j.biopsych.2005.02.006
  53. Chamberlain SR, Fineberg NA, Menzies LA, Blackwell AD, Bullmore ET, Robbins TW, et al. Impaired cognitive flexibility and motor inhibition in unaffected first-degree relatives of patients with obsessive-compulsive disorder. Am J Psychiatry 2007;164:335-338. https://doi.org/10.1176/ajp.2007.164.2.335
  54. Menzies L, Achard S, Chamberlain SR, Fineberg N, Chen CH, del Campo N, et al. Neurocognitive endophenotypes of obsessive-compulsive disorder. Brain 2007;130(Pt 12):3223-3236. https://doi.org/10.1093/brain/awm205
  55. Barch DM, Braver TS, Carter CS, Poldrack RA, Robbins TW. CNTRICS final task selection: executive control. Schizophr Bull 2009; 35:115-135. https://doi.org/10.1093/schbul/sbn154
  56. Xiao T, Xiao Z, Ke X, Hong S, Yang H, Su Y, et al. Response inhibition impairment in high functioning autism and attention deficit hyperactivity disorder: evidence from near-infrared spectroscopy data. PLoS One 2012;7:e46569. https://doi.org/10.1371/journal.pone.0046569
  57. Aron AR, Poldrack RA. The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biol Psychiatry 2005;57:1285-1292. https://doi.org/10.1016/j.biopsych.2004.10.026
  58. Chamberlain SR, Fineberg NA, Blackwell AD, Robbins TW, Sahakian BJ. Motor inhibition and cognitive flexibility in obsessive-compulsive disorder and trichotillomania. Am J Psychiatry 2006;163: 1282-1284. https://doi.org/10.1176/ajp.2006.163.7.1282
  59. Bush G, Valera EM, Seidman LJ. Functional neuroimaging of attention-deficit/hyperactivity disorder: a review and suggested future directions. Biol Psychiatry 2005;57:1273-1284. https://doi.org/10.1016/j.biopsych.2005.01.034
  60. Minshew NJ, Keller TA. The nature of brain dysfunction in autism: functional brain imaging studies. Curr Opin Neurol 2010;23:124-130. https://doi.org/10.1097/WCO.0b013e32833782d4
  61. Fornito A, Yucel M, Dean B, Wood SJ, Pantelis C. Anatomical abnormalities of the anterior cingulate cortex in schizophrenia: bridg ing the gap between neuroimaging and neuropathology. Schizophr Bull 2009;35:973-993. https://doi.org/10.1093/schbul/sbn025
  62. Milad MR, Rauch SL. Obsessive-compulsive disorder: beyond segregated cortico-striatal pathways. Trends Cogn Sci 2012;16:43-51. https://doi.org/10.1016/j.tics.2011.11.003
  63. Guo WB, Liu F, Xue ZM, Gao K, Wu RR, Ma CQ, et al. Altered white matter integrity in young adults with first-episode, treatment-naive, and treatment-responsive depression. Neurosci Lett 2012;522:139-144. https://doi.org/10.1016/j.neulet.2012.06.027