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Brain Structure and Function

, Volume 222, Issue 5, pp 2183–2192 | Cite as

Relationship among interthalamic adhesion size, thalamic anatomy and neuropsychological functions in healthy volunteers

  • Nishad R. Damle
  • Toshikazu Ikuta
  • Majnu John
  • Bart D. Peters
  • Pamela DeRosse
  • Anil K. Malhotra
  • Philip R. SzeszkoEmail author
Original Article

Abstract

The interthalamic adhesion (ITA) is an understudied neuroanatomical structure that forms a bridge of tissue connecting the thalamus of each hemisphere across the midline whose functional significance remains largely unknown. The likelihood of ITA absence has been reported in some studies to be increased in males, but findings have been inconsistent. We used magnetic resonance imaging to investigate the size and absence of the ITA and their relationship to thalamic volume, putative indices of white matter integrity (fractional anisotropy and mean diffusivity) within the anterior thalamic radiation and neuropsychological functions in 233 (129 M/104 F) healthy volunteers (age range 8–68). To ensure high reliability in this study two operators independently rated the absence of the ITA and measured its size for all individuals. The ITA was absent in 4% of all individuals with no sex differences in its absence. Females had greater ITA size compared to males overall with both groups demonstrating nonlinear age-associated changes across the age range examined. ITA size among females correlated significantly with thalamus volume and lower mean diffusivity in the anterior thalamic radiation. Path modeling indicated that ITA size statistically mediated the relationship between age and attention among females. Our findings provide evidence for sex differences in ITA size across the lifespan, which are associated with the surrounding thalamic anatomy and neuropsychological functions.

Keywords

Interthalamic adhesion Magnetic resonance imaging Diffusion tensor imaging Thalamus Sex effects 

Notes

Acknowledgements

This work was supported in part by Grants from the National Institute of Mental Health to Dr. Szeszko (R01 MH076995), the NSLIJ Research Institute General Clinical Research Center (M01 RR018535), an Advanced Center for Intervention and Services Research (P30 MH090590) and a Center for Intervention Development and Applied Research (P50 MH080173).

References

  1. Ahsan RL, Allom R, Gousias IS, Habib H, Turkheimer FE, Lemieux L et al (2007) Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus. Neuroimage 38:261–270. doi: 10.1016/j.neuroimage.2007.06.004 CrossRefPubMedGoogle Scholar
  2. Allen LS, Gorski RA (1991) Sexual dimorphism of the anterior commissure and massa intermedia of the human brain. J Comp Neurol 312(1):97–104CrossRefPubMedGoogle Scholar
  3. Baron RM, Kenny DA (1986) The moderator-mediator variable distinction in social psychological research: conceptual, strategic and statistical considerations. J Pers Soc Psychol 51:1173–1182CrossRefPubMedGoogle Scholar
  4. Booth T, Bastin ME, Penke L, Maniega SM, Murray C, Royle NA, Gow AJ, Corley J, Henderson RD, Hernández Mdel C, Starr JM, Wardlaw JM, Deary IJ (2013) Brain white matter tract integrity and cognitive abilities in community-dwelling older people: the Lothian Birth Cohort, 1936. Neuropsychology 27(5):595–607. doi: 10.1037/a0033354 (Epub 2013 Aug 12) CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bramen JE, Hranilovich JA, Dahl RE, Forbes EE, Chen J, Toga AW et al (2011) Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cereb Cortex 21:636–646. doi: 10.1093/cercor/bhq137 CrossRefPubMedGoogle Scholar
  6. Ceyhan M, Adapinar B, Aksaray G, Ozdemir F, Colak E (2008) Absence and size of massa intermedia in patients with schizophrenia and bipolar disorder. Acta Neuropsychiatry 20:193–198CrossRefGoogle Scholar
  7. Cheng S, Tan K, Bilston LE (2010) The effects of the interthalamic adhesion position on cerebrospinal fluid dynamics in the cerebral ventricles. J Biomech 43(3):579–582. doi: 10.1016/j.jbiomech.2009.10.002 (Epub 2009 Nov 5) CrossRefPubMedGoogle Scholar
  8. Choi MH, Kim JH, Yeon HW, Choi JS, Park JY, Jun JH, Lee BY, Kim HJ, Tack GR, Chung SC (2011) Effects of gender and age on anterior commissure volume. Neurosci Lett 500(2):92–94. doi: 10.1016/j.neulet.2011.06.010 (Epub 2011 Jun 15) CrossRefPubMedGoogle Scholar
  9. Cohen J, Cohen P (1983) Applied multiple regression/correlation analysis for the behavioral sciences. Taylor & Francis, Boca RatonGoogle Scholar
  10. Coscia DM, Narr KL, Robinson DG, Hamilton LS, Sevy S, Burdick KE et al (2009) Volumetric and shape analysis of the thalamus in first-episode schizophrenia. Hum Brain Mapp 30:1236–1245. doi: 10.1002/hbm.20595 CrossRefPubMedGoogle Scholar
  11. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980. doi: 10.1016/j.neuroimage.2006.01.021 CrossRefPubMedGoogle Scholar
  12. First MB, Spitzer RL, Gibbon M, Williams JBW (2002) Structured clinical interview for DSM-IV-TR axis I disorders, research version, non-patient edition (SCID-I/NP). Biometrics Research, New York State Psychiatric Institute, New YorkGoogle Scholar
  13. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C et al (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355CrossRefPubMedGoogle Scholar
  14. Fischl B, Salat DH, van der Kouwe AJ, Makris N, Segonne F, Quinn BT et al (2004) Sequence-independent segmentation of magnetic resonance images. Neuroimage 23:S69–S84. doi: 10.1016/j.neuroimage.2004.07.016 CrossRefPubMedGoogle Scholar
  15. Fjell AM, Walhovd KB (2010) Structural brain changes in aging: courses, causes and cognitive consequences. Rev Neurosci 21:187–221CrossRefPubMedGoogle Scholar
  16. Gruner P, Christian C, Robinson DG, Sevy S, Gunduz-Bruce H, Napolitano B, Bilder RM, Szeszko PR (2012) Pituitary volume in first-episode schizophrenia. Psychiatry Res 203(1):100–102. doi: 10.1016/j.pscychresns.2011.09.017 (Epub 2012 Aug 2) CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gur RC, Richard J, Calkins ME, Chiavacci R, Hansen JA, Bilker WB, Loughead J, Connolly JJ, Qiu H, Mentch FD, Abou-Sleiman PM, Hakonarson H, Gur RE (2012) Age group and sex differences in performance on a computerized neurocognitive battery in children age 8–21. Neuropsychology 26(2):251–265. doi: 10.1037/a0026712 (Epub 2012 Jan 16) CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hasegawa D, Yayoshi N, Fujita Y, Fujita M, Orima H (2005) Measurement of interthalamic adhesion thickness as a criteria for brain atrophy in dogs with and without cognitive dysfunction (dementia). Vet Radiol Ultrasound 46(6):452–457 (PubMed PMID: 16396259) CrossRefPubMedGoogle Scholar
  19. Hirayasu Y, Wada JA (1992) Convulsive seizures in rats induced by N-methyl-d-aspartate injection into the massa intermedia. Brain Res 577:36–40CrossRefPubMedGoogle Scholar
  20. Hughes EJ, Bond J, Svrckova P, Makropoulos A, Ball G, Sharp DJ et al (2012) Regional changes in thalamic shape and volume with increasing age. Neuroimage 63:1134–1142. doi: 10.1016/j.neuroimage.2012.07.043 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kamali A, Kramer LA, Hasan KM (2010) Feasibility of prefronto-caudate pathway tractography using high resolution diffusion tensor tractography data at 3T. J Neurosci Methods. 191(2):249–254. doi: 10.1016/j.jneumeth.2010.06.026 (Epub 2010 Jun 30) (PubMed PMID: 20600311; PubMed Central PMCID: PMC2924911) CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P et al (1997) Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36:980–988CrossRefPubMedGoogle Scholar
  23. Kline RB (2010) Principles and practice of structural equation modeling, 3rd edn. Guilford Press, New YorkGoogle Scholar
  24. Koolschijn PC, Crone EA (2013) Sex differences and structural brain maturation from childhood to early adulthood. Dev Cogn Neurosci 5:106–118. doi: 10.1016/j.dcn.2013.02.003 CrossRefPubMedGoogle Scholar
  25. Laslo P, Slobodan M, Nela P, Milos M, Rade P, Tatjana I (2005) Specific circular organization of the neurons of human interthalamic adhesion and of periventricular thalamic region. Int J Neurosci 115:669–679CrossRefPubMedGoogle Scholar
  26. Lee JS, Yoo SS, Cho SY, Ock SM, Lim MK, Panych LP (2006) Abnormal thalamic volume in treatment naive boys with Tourette syndrome. Acta Psychiatr Scand 113:64–67. doi: 10.1111/j.1600-0447.2005.00666.x CrossRefPubMedGoogle Scholar
  27. Luders E, Gaser C, Narr KL, Toga AW (2009) Why sex matters: brain size independent differences in gray matter distributions between men and women. J Neurosci 29(45):14265–14270. doi: 10.1523/JNEUROSCI.2261-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Malobabić S, Puskas L, Blagotić M (1987) Size and position of the human adhaesio interthalamica. Gegenbaurs Morphol Jahrb 133:175–180PubMedGoogle Scholar
  29. Malobabić S, Puskas L, Vujasković G (1990) Golgi morphology of the neurons in frontal sections of human interthalamic adhesion. Acta Anat (Basel) 139(3):234–238CrossRefGoogle Scholar
  30. Mohammadi MR, Hosseini SH, Golalipour MJ (2008) Morphometric measurements of the thalamus and interthalamic adhesion by MRI in the South-East of the Caspian Sea border. Neurosciences 13:272–275PubMedGoogle Scholar
  31. Nayak SB, Soumya KV (2010) Unusually large interthalamic adhesion and its clinical importance. Int J Anat Var 3:174–175Google Scholar
  32. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  33. O’Rahilly R, Müller F (1990) Ventricular system and choroid plexuses of the human brain during the embryonic period proper. Am J Anat 189:285–302CrossRefPubMedGoogle Scholar
  34. Park IA, Lee HY, Chung IH, Han YP, Shin TS (1993) A morphologic study of interthalamic adhesions in Korean Brains. Clin Anat 6:33–36CrossRefGoogle Scholar
  35. Peters BD, Ikuta T, DeRosse P, John M, Burdick KE, Gruner P, Prendergast DM, Szeszko PR, Malhotra AK (2014) Age-related differences in white matter tract microstructure are associated with cognitive performance from childhood to adulthood. Biol Psychiatry 75(3):248–256. doi: 10.1016/j.biopsych.2013.05.020 (Epub 2013 Jul 2) CrossRefPubMedGoogle Scholar
  36. Raz S, Goldstein R, Hopkins TL, Lauterbach MD, Shah F, Porter CL, Riggs WW, Magill LH, Sander CJ (1994) Sex differences in early vulnerability to cerebral injury and their neurodevelopmental implications. Psychobiology 22(3):244–253Google Scholar
  37. Rosales RK, Lemay MJ, Yakovlev PI (1968) The development and involution of the massa intermedia with regard to age and sex. J Neuropathol Exp Neurol 27:166PubMedGoogle Scholar
  38. Sen F, Ulubay H, Ozeksi P, Sargon MF, Tascioglu AB (2005) Morphometric measurements of the thalamus and interthalamic adhesion by MR imaging. Neuroanatomy 4:10–12Google Scholar
  39. Shimizu M, Fujiwara H, Hirao K, Namiki C, Fukuyama H, Hayashi T et al (2008) Structural abnormalities of the adhesio interthalamica and mediodorsal nuclei of the thalamus in schizophrenia. Schizophr Res 101:331–338. doi: 10.1016/j.schres.2007.12.486 CrossRefPubMedGoogle Scholar
  40. Sobel ME (1986) Some new results on indirect effects and their standard errors in covariance structure models. Sociol Methodol 16:159–186CrossRefGoogle Scholar
  41. Spalletta G, Fagioli S, Caltagirone C, Piras F (2013) Brain microstructure of subclinical apathy phenomenology in healthy individuals. Hum Brain Mapp 34(12):3193–3203. doi: 10.1002/hbm.22137 (Epub 2012 Jul 17) CrossRefPubMedGoogle Scholar
  42. Sullivan EV, Rosenbloom M, Serventi KL, Pfefferbaum A (2004) Effects of age and sex on volumes of the thalamus, pons, and cortex. Neurobiol Aging 25:185–192. doi: 10.1016/S0197-4580(03)00044-7 CrossRefPubMedGoogle Scholar
  43. Trzesniak C, Kempton MJ, Busatto GF, de Oliveira IR, Galvão-de Almeida A, Kambeitz J et al (2011) Adhesio interthalamica alterations in schizophrenia spectrum disorders: a systematic review and meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 35:877–886. doi: 10.1016/j.pnpbp.2010.12.024 (Epub 2011 Feb 16) CrossRefPubMedGoogle Scholar
  44. Van Der Werf YD, Tisserand DJ, Visser PJ, Hofman PA, Vuurman E, Uylings HB et al (2001) Thalamic volume predicts performance on tests of cognitive speed and decreases in healthy aging. A magnetic resonance imaging-based volumetric analysis. Brain Res Cogn Brain Res 11:377–385CrossRefGoogle Scholar
  45. Xie Y, Chen YA, De Bellis MD (2012) The relationship of age, gender, and IQ with the brainstem and thalamus in healthy children and adolescents: a magnetic resonance imaging volumetric study. J Child Neurol 27:325–331. doi: 10.1177/0883073811419260 CrossRefPubMedGoogle Scholar
  46. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128. doi: 10.1016/j.neuroimage.2006.01.015 CrossRefPubMedGoogle Scholar
  47. Zhou SY, Suzuki M, Hagino H, Takahashi T, Kawasaki Y, Nohara S et al (2003) Decreased volume and increased asymmetry of the anterior limb of the internal capsule in patients with schizophrenia. Biol Psychiatry 54:427–436CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Nishad R. Damle
    • 1
  • Toshikazu Ikuta
    • 2
  • Majnu John
    • 3
    • 4
    • 5
  • Bart D. Peters
    • 3
    • 4
  • Pamela DeRosse
    • 3
    • 4
    • 6
  • Anil K. Malhotra
    • 3
    • 4
    • 6
  • Philip R. Szeszko
    • 7
    • 8
    Email author
  1. 1.Purdue UniversityWest LafayetteUSA
  2. 2.Department of Communication Sciences and Disorders, School of Applied SciencesUniversity of MississippiOxfordUSA
  3. 3.Psychiatry ResearchZucker Hillside HospitalGlen OaksUSA
  4. 4.Center for Psychiatric NeuroscienceThe Feinstein Institute for Medical ResearchManhassetUSA
  5. 5.Department of MathematicsHofstra UniversityHempsteadUSA
  6. 6.Departments of Psychiatry and Molecular MedicineHofstra Northwell School of MedicineHempsteadUSA
  7. 7.James J. Peters Veterans Affairs Medical CenterMental Health Care CenterBronxUSA
  8. 8.Department of PsychiatryIcahn School of Medicine at Mount SinaiNew YorkUSA

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