Skip to main content

Advertisement

Log in

Claustral structural connectivity and cognitive impairment in drug naïve Parkinson’s disease

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

The claustrum is a thin grey matter structure which is involved in a wide brain network. Previous studies suggested a link between claustrum and Parkinson’s Disease (PD), showing how α-synuclein pathology may affect claustral neurons as well as how α-synuclein immunoreactivity may correlate with the onset of cognitive dysfunctions. Our aim is to investigate, via diffusion MRI, claustral structural network changes in drug naïve PD patients, with the goal to understand whether such changes may contribute to cognitive decline in PD. 15 drug naïve PD patients and 15 age-matched controls were enrolled; MR protocol was performed on a 3T scanner. Whole brain probabilistic tractography was obtained using Constrained Spherical Deconvolution (CSD) diffusion model. Connectivity matrices were estimated based on a robust anatomical parcellation of structural T1w images. In PD group, impaired subnetworks were correlated with psychological examinations. We found decreased claustral connectivity in PD patients compared to controls, especially with areas mainly involved in visuomotor and attentional systems. Moreover, we found a positive correlation between MoCA and density of pathways connecting ipsilaterally claustrum to left (r = 0.578, p = 0.021) and right (r = 0.640, p = 0.020) Pars Orbitalis. Our results support the hypothesis of claustral involvement in cognitive decline in drug naïve PD patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amaral, D. G., & Cowan, W. M. (1980). Subcortical afferents to the hippocampal formation in the monkey. The Journal of Comparative Neurology, 189, 573–591. https://doi.org/10.1002/cne.901890402.

    Article  CAS  PubMed  Google Scholar 

  • Amaral, D. G., & Insausti, R. (1992). Retrograde transport of D-[3H]-aspartate injected into the monkey amygdaloid complex. Experimental Brain Research, 88(2), 375–388.

    Article  CAS  Google Scholar 

  • Andersen, D. L. (1968). Some striatal connections to the claustrum. Experimental Neurology, 20(2):261-267 https://doi.org/10.1016/0014-4886(68)90100-3, 267.

  • Arikuni, T., & Kubota, K. (1985). Claustral and amygdaloid afferents to the head of the caudate nucleus in macaque monkeys. Neuroscience Research, 2(4), 239–254.

    Article  CAS  Google Scholar 

  • Arrigo, A., Mormina, E., Anastasi, G. P., Gaeta, M., Calamuneri, A., Quartarone, A., De Salvo, S., Bruschetta, D., Rizzo, G., Trimarchi, F., & Milardi, D. (2014). Constrained spherical deconvolution analysis of the limbic network in human, with emphasis on a direct cerebello-limbic pathway. Frontiers in Human Neuroscience, 8, 987. https://doi.org/10.3389/fnhum.2014.00987.

    Article  PubMed  PubMed Central  Google Scholar 

  • Arrigo, A., Calamuneri, A., Mormina, E., Gaeta, M., Quartarone, A., Marino, A., Anastasi, G. P., & Aragona, P. (2016). New insights in the optic radiations connectivity in the human brain. Investigative Ophthalmology & Visual Science, 57(1), 1–5. https://doi.org/10.1167/iovs.15-18082.

    Article  CAS  Google Scholar 

  • Arrigo, A., Mormina, E., Calamuneri, A., Gaeta, M., Granata, F., Marino, S., Anastasi, G. P., & Quartarone, A. (2017). Inter-hemispheric Claustral connections in human brain: A constrained spherical deconvolution-based study. Clinical Neuroradiology, 27, 275–281. https://doi.org/10.1007/s00062-015-0492-x.

    Article  CAS  PubMed  Google Scholar 

  • Baizer, J. S., Lock, T. M., & Youakim, M. (1997). Projections from the claustrum to the prelunate gyrus in the monkey. Experimental Brain Research, 113, 564–568.

    Article  CAS  Google Scholar 

  • Basser, P. J., Pajevic, S., Pierpaoli, C., Duda, J., & Aldroubi, A. (2000). In vivo fiber tractography using DT-MRI data. Magnetic Resonance in Medicine, 44, 625–632.

    Article  CAS  Google Scholar 

  • Beck, A. T., Steer, R. A., Brown, G. K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX. 1996: Psychological Corporation.

  • Behrens, T. E., & Sporns, O. (2012). Human connectomics. Current Opinion in Neurobiology, 22(1), 144–153. https://doi.org/10.1016/j.conb.2011.08.005.

    Article  CAS  PubMed  Google Scholar 

  • Besson, P., Dinkelacker, V., Valabregue, R., Thivard, L., Leclerc, X., Baulac, M., Sammler, D., Colliot, O., Lehéricy, S., & Samson, D. S. (2014). Structural connectivity differences in left and right temporal lobe epilepsy. NeuroImage, 100, 135–144. https://doi.org/10.1016/j.neuroimage.2014.04.071.

    Article  PubMed  Google Scholar 

  • Bijttebier, S., Caeyenberghs, K., van den Ameele, H., Achten, E., Rujescu, D., Titeca, K., & Van Heeringen, C. (2015). The vulnerability to suicidal behavior is associated with reduced connectivity strength. Frontiers in Human Neuroscience, 9, 632. https://doi.org/10.3389/fnhum.2015.00632.

    Article  PubMed  PubMed Central  Google Scholar 

  • Biundo, R., Weis, L., Bostantjopoulou, S., Stefanova, E., Falup-Pecurariu, C., Kramberger, M. G., Geurtsen, G. J., Antonini, A., Weintraub, D., & Aarsland, D. (2016). MMSE and MoCA in Parkinson's disease and dementia with Lewy bodies: A multicenter 1-year follow-up study. Journal of Neural Transmissions (Vienna), 123(4), 431–438. https://doi.org/10.1007/s00702-016-1517-6.

    Article  CAS  Google Scholar 

  • Braak, H., Sastre, M., & Del Tredici, K. (2007). Development of alpha-synuclein immunoreactive astrocytes in the forebrain parallels stages of intraneuronal pathology in sporadic Parkinson's disease. Acta Neuropathologica, 114(3), 231–241.

    Article  CAS  Google Scholar 

  • Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10, 186–198.

    Article  CAS  Google Scholar 

  • Cacciola, A., Milardi, D., Anastasi, G. P., Basile, G. A., Ciolli, P., Irrera, M., Cutroneo, G., Bruschetta, D., Rizzo, G., Mondello, S., Bramanti, P., & Quartarone, A. (2016). A directo Cortico-Nigral pathway as revealed by constrained spherical deconvolution Tractography in humans. Frontiers in Human Neuroscience, 10. https://doi.org/10.3389/fnhum.2016.00374.

  • Cacciola, A., Calamuneri, A., Milardi, D., Mormina, E., Chillemi, G., Marino, S., Naro, A., Rizzo, V., Anastasi, G. P., & Quartarone, A. (2017). A Connectomic analysis of the human basal ganglia network. Frontiers in Neuroanatomy, 11, 85. https://doi.org/10.3389/fnana.2017.00085.

    Article  PubMed  PubMed Central  Google Scholar 

  • Camicioli, R. M., Korzan, J. R., Foster, S. L., Fisher, N. J., Emery, D. J., Bastos, A. C., & Hanstock, C. C. (2004). Posterior cingulate metabolic changes occur in Parkinson's disease patients without dementia. Neuroscience Letters, 354(3), 177–180.

    Article  CAS  Google Scholar 

  • Chaudhuri, K. R., & Schapira, A. H. (2009). Non-motor symptoms of Parkinson's disease: Dopaminergic pathophysiology and treatment. Lancet Neurology, 8(5), 464–474. https://doi.org/10.1016/S1474-4422(09)70068-7.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y., Pressman, P., Simuni, T., Parrish, T. B., & Gitelman, D. R. (2015). Effects of acute levodopa challenge on resting cerebral blood flow in Parkinson's disease patients assessed using pseudo-continuous arterial spin labeling. PeerJ, 3, e1381. https://doi.org/10.7717/peerj.1381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Compta, Y., Parkkinen, L., O’sullivan, S. S., Vandrovcova, J., Holton, J. L., Collins, C., Lashley, T., Kallis, C., Williams, D. R., & de Silva, R. (2011). Lewy-and Alzheimer-type pathologies in Parkinson’s disease dementia: Which is more important? Brain, 134(5), 1493–1505. https://doi.org/10.1093/brain/awr031.

    Article  PubMed  PubMed Central  Google Scholar 

  • Crick, F. C., & Koch, C. (2005). What is the function of the claustrum? Philosophical Transaction of the Royal Society B Biological, 360(1458), 1271–1279. https://doi.org/10.1098/rstb.2005.1661.

    Article  Google Scholar 

  • Culham, J. C., Cavina-Pratesi, C., & Singhal, A. (2006). The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? Neuropsychologia, 44(13), 2668–2684.

    Article  Google Scholar 

  • Dalrymple-Alford, J. C., MacAskill, M. R., Nakas, C. T., Livingston, L., Graham, C., Crucian, G. P., Melzer, T. R., Kirwan, J., Keenan, R., Wells, S., Porter, R. J., Watts, R., & Anderson, T. J. (2010). The MoCA well-suited screen for cognitive impairment in Parkinson disease. Neurology, 75(19), 1717–1725.

    Article  CAS  Google Scholar 

  • Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. L., Dale, A. M., Maguire, R. P., Hyman, B. T., Albert, M. S., & Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021.

    Article  PubMed  Google Scholar 

  • Diederich, N. J., Stebbins, G., Schiltz, C., & Goetz, C. G. (2014). Are patients with Parkinson’s disease blind to blindsight? Brain, 137, 1838–1849. https://doi.org/10.1093/brain/awu094.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dušek, P., Jech, R., Sieger, T., Vymazal, J., Růžička, E., Wackermann, J., & Mueller, K. (2012). Abnormal activity in the precuneus during time perception in Parkinson's disease: An fMRI study. PLoS One, 7(1), e29635. https://doi.org/10.1371/journal.pone.0029635.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edelstein, L. R., & Denaro, F. J. (2004). The claustrum: A historical review of its anatomy, physiology, cytochemistry and functional significance. Cellular and molecular biology (Noisy-le-grand), 50(6), 675–702.

    CAS  Google Scholar 

  • Fahn, S., Elton, R. L. (1987) and Members od UPDRS Development Committee. The Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M, editors. Recent Developments in Parkinson’s Disease, Macmillan Healthcare Information; Florham Park. p.153–163.

  • Farquharson, S., Tournier, J. D., Calamante, F., Fabinyi, G., Schneider-Kolsky, M., Jackson, G. D., & Connelly, A. (2013). White matter fiber tractography: Why we need to move beyond DTI: Clinical article. Journal of Neurosurgery, 118(6), 1367–1377. https://doi.org/10.3171/2013.2.JNS121294.

    Article  PubMed  Google Scholar 

  • Fengler, S., Kessler, J., Timmermann, L., Zapf, A., Elben, S., Wojtecki, L., Tucha, O., & Kalbe, E. (2016). Screening for cognitive impairment in Parkinson's disease: Improving the diagnostic utility of the MoCA through subtest weighting. PLoS One, 11(7), e0159318. https://doi.org/10.1371/journal.pone.0159318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filoteo, J. V., Reed, J. D., Litvan, I., & Harrington, D. L. (2014). Volumetric correlates of cognitive functioning in nondemented patients with Parkinson's disease. Movement Disorders, 29(3), 360–367. https://doi.org/10.1002/mds.25633.

    Article  PubMed  Google Scholar 

  • Fiorenzato, E., Weis, L., Falup-Pecurariu, C., Diaconu, S., Siri, C., Reali, E., Pezzoli, G., Bisiacchi, P., Antonini, A., & Biundo, R. (2016). Montreal cognitive assessment (MoCA) and mini-mental state examination (MMSE) performance in progressive supranuclear palsy and multiple system atrophy. Journal of Neural Transmission, 123, 1435–1442. https://doi.org/10.1007/s00702-016-1589-3.

    Article  PubMed  Google Scholar 

  • Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Sègonne, F., Salata, D. H., Busa, E., Seidman, L. J., Goldstein, J., Kennedy, D., Caviness, V., Makris, N., Rosen, B., & Dale, A. M. (2004). Automatically Parcellating the human cerebral cortex. Cerebral Cortex, 14, 11–22.

    Article  Google Scholar 

  • Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1978). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198.

    Article  Google Scholar 

  • Glerean, E., Pan, R. K., Salmi, J., Bernard, B., Merkitch, D., deToledo-Morrell, L., & Goetz, C. G. (2016). Reorganization of functionally connected brain subnetworks in high-functioning autism. Human Brain Mapping, 37, 1066–1079.

    Article  Google Scholar 

  • Gorges, M., Müller, H. P., Lulé, D., Ludolph, A. C., Pinkhardt, E. H., & Kassubek, J. (2013). Functional connectivity within the default mode network is associated with saccadic accuracy in Parkinson's disease: A resting-state FMRI and videooculographic study. Brain Connectivity, 3(3), 265–272. https://doi.org/10.1089/brain.2013.0146.

    Article  PubMed  Google Scholar 

  • Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: Onset, progression, and mortality. Neurology, 17, 427–442.

    Article  CAS  Google Scholar 

  • Huang, C., Tang, C., Feigin, A., Lesser, M., Ma, Y., Pourfar, M., Dhawan, V., & Eidelberg, D. (2007). Changes in network activity with the progression of Parkinson's disease. Brain, 130(Pt 7), 1834–1846.

    Article  Google Scholar 

  • Hughes, A. J., Daniel, S. E., Kilford, L., & Lees, A. J. (1992). Accuracy of clinical diagnosis of idiopathic Parkinson's disease: A clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery and Psychiatry, 55(3), 181–184.

    Article  CAS  Google Scholar 

  • Insausti, R., Amaral, D. G., & Cowan, W. M. (1987). The entorhinal cortex of the monkey: III. Subcortical afferents. The Journal of Comparative Neurology, 264, 396–408.

    Article  CAS  Google Scholar 

  • Ito, K., Nagano-Saito, A., Kato, T., Arahata, Y., Nakamura, A., Kawasumi, Y., Hatano, K., Abe, Y., Yamada, T., Kachi, T., & Brooks, D. J. (2002). Striatal and extrastriatal dysfunction in Parkinson’s disease with dementia: A 6-[18F]fluoro-l-dopa PET study. Brain, 125(6), 1358–1365. https://doi.org/10.1093/brain/awf134.

    Article  PubMed  Google Scholar 

  • Jellinger, K. A. (2009). A critical evaluation of current staging of alpha-synuclein pathology in Lewy body disorders. Biochimica et Biophysica Acta, 1792(7), 730–740. https://doi.org/10.1016/j.bbadis.2008.07.006.

    Article  CAS  PubMed  Google Scholar 

  • Kalaitzakis, M. E., Pearce, R. K. B., & Gentleman, S. M. (2009). Clinical correlates of pathology in the claustrum in Parkinson's disease and dementia with Lewy bodies. Neuroscience Letters, 461(1), 12–15. https://doi.org/10.1016/j.neulet.2009.05.083.

    Article  CAS  PubMed  Google Scholar 

  • Kalia, L. V., & Lang, A. E. (2015). Parkinson’s disease. The Lancet, 386(9996), 896–912. https://doi.org/10.1016/S0140-6736(14)61393-3.

    Article  CAS  Google Scholar 

  • Kamagata, K., Motoi, Y., Abe, O., Shimoji, K., Hori, M., Nakanishi, A., Sano, T., Kuwatsuru, R., Aoki, S., & Hattori, N. (2012). White matter alteration of the cingulum in Parkinson disease with and without dementia: Evaluation by diffusion tensor tract-specific analysis. American Journal of Neuroradiology, 33(5), 890–895. https://doi.org/10.3174/ajnr.A2860.

    Article  CAS  PubMed  Google Scholar 

  • Kawashima, R., Roland, P. E., & O'Sullivan, B. T. (1995). Functional anatomy of reaching and visuomotor learning: A positron emission tomography study. Cerebral Cortex, 5(2), 111–122.

    Article  CAS  Google Scholar 

  • Kievit, J., & Kuypers, H. G. (1975). Subcortical afferents to the frontal lobe in the rhesus monkey studied bymeans of retrograde horseradish peroxidase transport. Brain Research, 85, 261–266.

    Article  CAS  Google Scholar 

  • Kosaka, K. (1978). Lewy bodies in cerebral cortex, report of three cases. Acta Neuropathologica, 42, 127–134.

    Article  CAS  Google Scholar 

  • LeVay, S., & Sherk, H. (1981). The visual claustrum of the cat. I. Structure and connections. Journal of Neuroscience, 1(9), 956–980.

    Article  CAS  Google Scholar 

  • Lewis, S. J. G., Foltynie, T., Blackwell, A. D., Robbins, T. W., Owen, A. M., & Barker, R. A. (2005). Heterogeneity of Parkinson’s disease in the early clinical stages using a data driven Approach. Journal of Neurology, Neurosurgery & Psychiatry, 76(3), 343–348. https://doi.org/10.1136/jnnp.2003.033530.

    Article  CAS  Google Scholar 

  • Li, C., Huang, B., Zhang, R., Ma, Q., Yang, W., Wang, L., Wang, L., Xu, Q., Feng, J., Liu, L., Zhang, Y., & Huang, R. (2017). Impaired topological architecture of brain structural networks in idiopathic Parkinson’s disease: A DTI study. Brain Imaging and Behavior, 11(1), 113–128. https://doi.org/10.1007/s11682-015-9501-6.

    Article  PubMed  Google Scholar 

  • Liscovitch, N., & French, L. (2014). Differential co-expression between α-Synuclein and IFN-γ signaling genes across development and in Parkinson's disease. PLoS One, 9(12), e115029. https://doi.org/10.1371/journal.pone.0115029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lou, X. Y., Chen, G. B., Yan, L., Ma, J. Z., Zhu, J., Elston, R. C., & Li, M. D. (2007). A generalized combinatorial approach for detecting Gene-by-gene and gene-by-environment interactions with application to nicotine dependence. American Journal of Human Genetics, 80, 1125–1137.

    Article  CAS  Google Scholar 

  • Martin, W. R., Wieler, M., Gee, M., & Camicioli, R. (2009). Temporal lobe changes in early, untreated Parkinson's disease. Movement Disorders, 24(13), 1949–1954. https://doi.org/10.1002/mds.22680.

    Article  PubMed  Google Scholar 

  • McNamee, R. (2005). Regression modelling and other methods to control confounding. Occupational and Enviromental Medicine, 62, 500–506.

    Article  CAS  Google Scholar 

  • Meireles, J., & Massano, J. (2012). Cognitive impairment and dementia in Parkinson’s disease: Clinical features, diagnosis, and management. Frontiers in Neurology, 3. https://doi.org/10.3389/fneur.2012.00088.

  • Milardi, D., Bramanti, P., Milazzo, C., Finocchio, G., Arrigo, A., Santoro, G., Trimarchi, F., Quartarone, A., Anastasi, G., & Gaeta, M. (2015). Cortical and subcortical connections of the human claustrum revealed in vivo by constrained spherical deconvolution tractography. Cerebral Cortex, 25(2), 406–414. https://doi.org/10.1093/cercor/bht231.

    Article  PubMed  Google Scholar 

  • Mito, Y., Yoshida, K., Yabe, I., Makino, K., Hirotami, M., Tashiro, K., Kikuchi, S., & Sasaki, H. (2005). Brain 3D-SSP SPECT analysis in dementia with Lewy bodies, Parkinson's disease with and without dementia, and Alzheimer's disease. Clinical Neurology and Neurosurgery, 107(5), 396–403.

    Article  Google Scholar 

  • Mori, S., & van Zijl, P. C. M. (2002). Fiber tracking: Principles and strategies – A technical review. NMR in Biomedicine, 15, 468–480. https://doi.org/10.1002/nbm.781.

    Article  PubMed  Google Scholar 

  • Mormina, E., Arrigo, A., Calamuneri, A., Granata, F., Quartarone, A., Ghilardi, M. F., Inglese, M., Di Rocco, A., Milardi, D., Anastasi, G. P., & Gaeta, M. (2015a). Diffusion tensor imaging parameters’ changes of cerebellar hemispheres in Parkinson’s disease. Neuroradiology, 57, 327–334. https://doi.org/10.1007/s00234-014-1473-5.

    Article  PubMed  Google Scholar 

  • Mormina, E., Longo, M., Arrigo, A., Alafaci, C., Tomasello, F., Calamuneri, A., Marino, S., Gaeta, M., Vinci, S. L., & Granata, F. (2015b). Tractography of corticospinal tract and arcuate fasciculus in high-grade gliomas performed by constrained spherical deconvolution: Qualitative and quantitative analysis. American Journal of Neuroradiology, 36(10), 1853–1858. https://doi.org/10.3174/ajnr.A4368.

    Article  CAS  PubMed  Google Scholar 

  • Morys, J., Bobinski, M., Wegiel, J., Wisniewski, H. M., & Narkiewicz, O. (1996). Alzheimer’s disease severely affects areas of the claustrum connected with the entorhinal cortex. Journal für Hirnforschung, 37, 173–180.

    CAS  PubMed  Google Scholar 

  • Naghavi, H. R., Eriksson, J., Larsson, A., & Nyberg, L. (2007). The claustrum/insula region integrates conceptually related sounds and pictures. Neuroscience Letters, 422(1), 77–80.

    Article  CAS  Google Scholar 

  • Nasreddine, Z. S., Phillips, N. A., Bédirian, V., Phillips, N. A., Bèdirian, V., Charbonneau, S., Whitehead, V., Collin, I., Cummings, J. L., & Chertkow. (2005). The Montreal cognitive assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695–699.

    Article  Google Scholar 

  • Nombela, C., Rowe, J. B., Winder-Rhodes, S. E., Hampshire, A., Owen, A. M., Breen, D. P., Suncan, G. W., Khoo, T. K., Yarnali, A. J., Firbank, M. J., Chinnery, P. F., Robbins, T. W., O’Brien, J. T., Brooks, D. J., & Burn, D. J. (2014). Genetic impact on cognition and brain function in newly diagnosed Parkinson's disease: ICICLE-PD study. Brain, 137(Pt 10), 2743–2758. https://doi.org/10.1093/brain/awu201.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogomori, K., Kitamoto, T., Tateishi, J., Sato, Y., Suetsugu, M., & Abe, M. (1989). Beta-protein amyloid is widely distributed in the central nervous system of patients with Alzheimer’s disease. American Journal of Pathology, 134, 243–251.

    CAS  PubMed  Google Scholar 

  • Parsons, M. W., Harrington, D. L., & Rao, S. M. (2005). Distinct neural systems underlie learning visuomotor and spatial representations of motor skills. Human Brain Mapping, 24(3), 229–247.

    Article  Google Scholar 

  • Pearson, R. C., Brodal, P., Gatter, K. C., & Powell, T. P. (1982). The organization of the connections between the cortex and the claustrum in the monkey. Brain Research, 234, 435–444.

    Article  CAS  Google Scholar 

  • Poewe, W. (2008). Non-motor symptoms in Parkinson’s disease. European Journal of Neurology, 15(Suppl 1), 14–20. https://doi.org/10.1111/j.1468-1331.2008.02056.x.

    Article  PubMed  Google Scholar 

  • Rektor, I., Svátková, A., Vojtíšek, L., Zikmundová, I., Vaníček, J., Király, A., & Szabó, N. (2018). White matter alterations in Parkinson's disease with normal cognition precede grey matter atrophy. PLoS One, 13(1), e0187939. https://doi.org/10.1371/journal.pone.0187939.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remedios, R., Logothetis, N. K., & Kayser, C. (2014). A role of the claustrum in auditory scene analysis by reflecting sensory change. Frontiers in Systems Neuroscience, 8, 44. https://doi.org/10.3389/fnsys.2014.00044.

    Article  PubMed  PubMed Central  Google Scholar 

  • Roalf, D. R., Moberg, P. J., Xie, S. X., Wolk, D. A., Moelter, S. T., & Arnold, S. E. (2013). Comparative accuracies of two common screening instruments for classification of Alzheimer's disease, mild cognitive impairment, and healthy aging. Alzheimer's & Dementia, 9(5), 529–537. https://doi.org/10.1016/j.jalz.2012.10.001.

    Article  Google Scholar 

  • Roquet, D., Noblet, V., Anthony, P., Philippi, N., Demuynck, C., Cretin, B., Martin-Hunyadi, C., Loureiro de Sousa, P., & Blanc, F. (2017). Insular atrophy at the prodromal stage of dementia with Lewy bodies: A VBM DARTEL study. Scientific Reports, 7(1), 9437. https://doi.org/10.1038/s41598-017-08667-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. NeuroImage, 52, 1059–1069.

    Article  Google Scholar 

  • Selikhova, M., Williams, D. R., Kempster, P. A., Holton, J. L., Revesz, T., & Lees, A. J. (2009). A Clinico-pathological study of subtypes in Parkinson’s disease. Brain, 132(11), 2947–2957. https://doi.org/10.1093/brain/awp234.

    Article  CAS  PubMed  Google Scholar 

  • Shao, N., Yang, J., & Shang, H. (2015). Voxelwise meta-analysis of gray matter anomalies in Parkinson variant of multiple system atrophy and Parkinson's disease using anatomic likelihood estimation. Neuroscience Letters, 587, 79–86. https://doi.org/10.1016/j.neulet.2014.12.007.

    Article  CAS  PubMed  Google Scholar 

  • Sherk, H., & LeVay, S. (1981). The visual claustrum of the cat. III. Receptive field properties. Journal of Neuroscience, 1(9), 993–1002.

    Article  CAS  Google Scholar 

  • Shima, K., Hoshi, E., & Tanji, J. (1996). Neuronal activity in the claustrum of the monkey during performance of multiple movements. Journal of Neurophysiology, 76(3), 2115–2119.

    Article  CAS  Google Scholar 

  • Shipp, S., Blanton, M., & Zeki, S. (1998). A visuo-somatomotor pathway through superior parietal cortex in the macaque monkey: Cortical connections of areas V6 and V6A. European Journal of Neuroscience, 10, 3171–3193.

    Article  CAS  Google Scholar 

  • Simuni, T., & Sethi, K. (2008). Nonmotor manifestations of Parkinson’s disease. Annals of Neurology, 64(Suppl 2), S65–S80. https://doi.org/10.1002/ana.21472.

    Article  PubMed  Google Scholar 

  • Smith, J. B., & Alloway, K. D. (2010). Functional specificity of claustrum connections in the rat: Interhemispheric communication between specific parts of motor cortex. Journal of Neuroscience, 30(50), 16832–16844. https://doi.org/10.1523/JNEUROSCI.4438-10.2010.

    Article  CAS  PubMed  Google Scholar 

  • Smith, J. B., & Alloway, K. D. (2014). Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Frontiers in Systems Neuroscience, 8, 93. https://doi.org/10.3389/fnsys.2014.00093.

    Article  PubMed  PubMed Central  Google Scholar 

  • Smythies, J. (2015). On the function of object cells in the claustrum—Key components in information processing in the visual system? Frontiers in Cellular Neuroscience, 9. https://doi.org/10.3389/fncel.2015.00443.

  • Smythies, J., Edelstein, L., & Ramachandran, V. (2012). Hypotheses relating to the function of the claustrum. Frontiers in Integrative Neuroscience, 6, 53. https://doi.org/10.3389/fnint.2012.00053.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanné-Gariépy, J., Boussaoud, D., & Rouiller, E. M. (2002). Projections of the claustrum to the primary motor, premotor, and prefrontal cortices in the macaque monkey. The Journal of Comparative Neurology, 454(2), 140–157.

    Article  Google Scholar 

  • Torgerson, C. M., & Van Horn, J. D. (2014). A case study in connectomics: The history, mapping, and connectivity of the claustrum. Frontiers in Neoroinformatics, 8, 83. https://doi.org/10.3389/fninf.2014.00083.

    Article  Google Scholar 

  • Torgerson, C. M., Irimia, A., Goh, S. Y., & Van Horn, J. D. (2015). The DTI connectivity of the human claustrum. Human Brain Mapping, 36(3), 827–838.

    Article  Google Scholar 

  • Tournier, J. D., Calamante, F., & Connelly, A. (2007). Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution. NeuroImage, 35(4), 1459–1472.

    Article  Google Scholar 

  • Tournier, J. D., Yeh, C. H., Calamante, F., Cho, K. H., Connelly, A., & Lin, C. P. (2008). Resolving crossing fibres using constrained spherical deconvolution: Validation using diffusion-weighted imaging phantom data. NeuroImage, 42(2), 617–625. https://doi.org/10.1016/j.neuroimage.2008.05.002.

    Article  PubMed  Google Scholar 

  • Trzepacz, P. T., Hochstetler, H., Wang, S., Walker, B., & Saykin, A. J. (2015). Alzheimer’s Disease Neuroimaging Initiative. Relationship between the Montreal cognitive assessment and mini-mental state examination for assessment of mild cognitive impairment in older adults. BMC Geriatrics, 15, 107. https://doi.org/10.1186/s12877-015-0103-3.

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Eimeren, T., Monchi, O., Ballanger, B., & Strafella, A. P. (2009). Dysfunction of the default mode network in Parkinson disease: A functional magnetic resonance imaging study. Archives of Neurology, 66(7), 877–883. https://doi.org/10.1001/archneurol.2009.97.

    Article  PubMed  PubMed Central  Google Scholar 

  • Webster, M. J., Bachevalier, J., & Ungerleider, L. G. (1993). Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. The Journal of Comparative Neurology, 335(1), 73–91.

    Article  CAS  Google Scholar 

  • Yamamoto, R., Iseki, E., Murayamam, N., Minegishi, M., Marui, W., Togo, T., Katsuse, O., Kosaka, K., Kato, M., Iwatsubo, T., & Arai, T. (2007). Correlation in Lewy pathology between the claustrum and visual areas in brains of dementia with Lewybodies. Neuroscience Letters, 415, 219–224.

    Article  CAS  Google Scholar 

  • Yao, N., Shek-Kwan, C. R., Cheung, C., Pang, S., Lau, K. K., Suckling, H., Rowe, J. B., Yu, K., Ka-Fung, Mak. H., Chua, S., Ho, S. L., McAlonan, G. M. (2014). The default mode network is disrupted in Parkinson's disease with visual hallucinations. Human Brain Mapping, 35(11): 5658–5666. https://doi.org/10.1002/hbm.22577.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessandro Calamuneri.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(DOCX 24 kb)

ESM 2

(DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arrigo, A., Calamuneri, A., Milardi, D. et al. Claustral structural connectivity and cognitive impairment in drug naïve Parkinson’s disease. Brain Imaging and Behavior 13, 933–944 (2019). https://doi.org/10.1007/s11682-018-9907-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-018-9907-z

Keywords

Navigation