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24.11.2020 | Original Article

Different functional connectivity modes of the right fronto-insular cortex in akinetic-rigid and tremor-dominant Parkinson’s disease

verfasst von: Juan Wang, Yalian Shen, Juan Peng, Anran Wang, Xiaolin Wu, Xiaocui Chen, Jinjin Liu, Min Wei, Dezhi Zou, Yu Han, Oumei Cheng

Erschienen in: Neurological Sciences | Ausgabe 7/2021

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Abstract

Background

Patients with akinetic-rigid Parkinson’s disease (AR-PD) are more prone to cognitive decline and depressive symptoms than tremor-dominant PD (TD-PD) patients. The right fronto-insular cortex (rFIC), as a key node of salience network, plays a critical role in the switching between central executive network and default mode network. In this study, we explored the functional connectivity mode of rFIC with triple-brain networks, namely default mode network, salience network, and central executive network, in two motor subtypes of PD.

Methods

We recruited 44 PD patients (including the TD-PD group and AR-PD group) and 18 age-matched healthy controls (HCs). We performed functional connectivity (FC) analysis of resting-state functional MRI.

Results

Compared with TD-PD, decreased FC were found in the right insular cortex and bilateral anterior cingulate gyrus in AR-PD. Compared with HCs, decreased FC in the bilateral insula, the anterior cingulate gyrus, the precentral gyrus, and the right medial frontal gyrus were found; therein, the FC value of rFIC-precentral gyrus was positively correlated with the Unified Parkinson’s Disease Rating Scale-II score in AR-PD (p = 0.0482, r = 0.4162). While TD-PD showed decreased FC in the left insula as well as bilateral anterior cingulate gyrus when compared with HCs, and the FC value of the rFIC-left insula was positively correlated with its Hamilton Depression Rating Scale score (p = 0.02, r = 0.50).

Conclusion

The functional connectivity mode of rFIC in AR-PD differed from that in TD-PD. The decreased rFIC FC with the other nodes of salience network might be a potential indicator for AR-PD patients prone to develop cognitive decline and depressive symptoms.

Rajput AH, Voll A, Rajput ML, Robinson CA, Rajput A (2009) Course in Parkinson disease subtypes: a 39-year clinicopathologic study. Neurology 73(3):206–212PubMedCrossRef

Lewis MM, Du G, Sen S et al (2011) Differential involvement of striato- and cerebello-thalamo-cortical pathways in tremor- and akinetic/rigid-predominant Parkinson’s disease. Neuroscience 177:230–239PubMedCrossRef

Zaidel A, Arkadir D, Israel Z, Bergman H (2009) Akineto-rigid vs. tremor syndromes in Parkinsonism. Curr Opin Neurol 22(4):387–393PubMedCrossRef

Reijnders JS, Ehrt U, Lousberg R et al (2009) The association between motor subtypes and psychopathology in Parkinson’s disease. Parkinsonism Relat Disord 15(5):379–382PubMedCrossRef

Vakil EHerishanu-Naaman S. (1998) Declarative and procedural learning in Parkinson’s disease patients having tremor or bradykinesia as the predominant symptom. Cortex 34(4):611–620CrossRef

Moustafa AA, Peter B, Eissa AM et al (2013) The effects of clinical motor variables and medication dosage on working memory in Parkinson’s disease. Brain Cogn 82(2):137–145PubMedCrossRef

Moustafa AA, Krishna R, Eissa AM, Hewedi DH (2013) Factors underlying probabilistic and deterministic stimulus-response learning performance in medicated and unmedicated patients with Parkinson’s disease. Neuropsychology 27(4):498–510PubMedCrossRef

van Uem JM, Marinus J, Canning C et al (2016) Health-related quality of life in patients with Parkinson’s disease--a systematic review based on the ICF model. Neurosci Biobehav Rev 61:26–34PubMedCrossRef

Schrag A, Jahanshahi M, Quinn N (2000) What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry 69(3):308–312PubMedPubMedCentralCrossRef

10.

Menon V (2011) Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci 15(10):483–506PubMedCrossRef

11.

Sheline YI, Barch DM, Price JL, Rundle MM, Vaishnavi SN, Snyder AZ, Mintun MA, Wang S, Coalson RS, Raichle ME (2009) The default mode network and self-referential processes in depression. Proc Natl Acad Sci U S A 106(6):1942–1947PubMedPubMedCentralCrossRef

12.

Fox M, DRaichle M (2007) E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711PubMedCrossRef

13.

Cai W, Chen T, Ryali S, Kochalka J, Li CSR, Menon V (2016) Causal interactions within a frontal-cingulate-parietal network during cognitive control: convergent evidence from a multisite-multitask investigation. Cereb Cortex 26(5):2140–2153PubMedCrossRef

14.

Karunanayaka PR, Lee EY, Lewis MM, Sen S, Eslinger PJ, Yang QX, Huang X (2016) Default mode network differences between rigidity- and tremor-predominant Parkinson’s disease. Cortex 81:239–250PubMedPubMedCentralCrossRef

15.

Hou Y, Luo C, Yang J, Ou R, Liu W, Song W, Gong Q, Shang H (2017) Default-mode network connectivity in cognitively unimpaired drug-naïve patients with rigidity-dominant Parkinson’s disease. J Neurol 264(1):152–160PubMedCrossRef

16.

Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356PubMedPubMedCentralCrossRef

17.

Allman JM, Watson KK, Tetreault NA, Hakeem AY (2005) Intuition and autism: a possible role for Von Economo neurons. Trends Cogn Sci 9(8):367–373PubMedCrossRef

18.

Menon VUddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5–6):655–667CrossRef

19.

Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci U S A 105(34):12569–12574PubMedPubMedCentralCrossRef

20.

Poeppl TB, Donges MR, Mokros A et al (2019) A view behind the mask of sanity: meta-analysis of aberrant brain activity in psychopaths. Mol Psychiatry 24(3):463–470PubMedCrossRef

21.

He X, Qin W, Liu Y, Zhang X, Duan Y, Song J, Li K, Jiang T, Yu C (2013) Age-related decrease in functional connectivity of the right fronto-insular cortex with the central executive and default-mode networks in adults from young to middle age. Neurosci Lett 544(24):74–79PubMedCrossRef

22.

Farb NA, Segal Z VAnderson A K. (2013) Attentional modulation of primary interoceptive and exteroceptive cortices. Cereb Cortex 23(1):114–126PubMedCrossRef

23.

Marinus J, Zhu K, Marras C et al (2018) Risk factors for non-motor symptoms in Parkinson’s disease. Lancet Neurol 17(6):559–568PubMedCrossRef

24.

Moustafa A, APoletti M (2013) Neural and behavioral substrates of subtypes of Parkinson’s disease. Front Syst Neurosci 7(7):117PubMedPubMedCentral

25.

Rajput DR (1993) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 56(8):938–939PubMedPubMedCentralCrossRef

26.

Kang GA, Bronstein JM, Masterman DL, Redelings M, Crum JA, Ritz B (2005) Clinical characteristics in early Parkinson’s disease in a central California population-based study. Mov Disord 20(9):1133–1142PubMedPubMedCentralCrossRef

27.

Vervoort G, Alaerts K, Bengevoord A, Nackaerts E, Heremans E, Vandenberghe W, Nieuwboer A (2016) Functional connectivity alterations in the motor and fronto-parietal network relate to behavioral heterogeneity in Parkinson’s disease. Parkinsonism Relat Disord 24:48–55PubMedCrossRef

28.

Ya-Ting C, Cheng-Hsien L, Ming-Kung W et al (2017) Salience network and depressive severities in Parkinson’s disease with mild cognitive impairment: a structural covariance network analysis. Front Aging Neurosci 9:417

29.

Aracil-Bolaños I, Sampedro F, Marín-Lahoz J, Horta-Barba A, Martínez-Horta S, Botí M, Pérez-Pérez J, Bejr-Kasem H, Pascual-Sedano B, Campolongo A, Izquierdo C, Gironell A, Gómez-Ansón B, Kulisevsky J, Pagonabarraga J (2019) A divergent breakdown of neurocognitive networks in Parkinson’s disease mild cognitive impairment. Hum Brain Mapp 40(11):3233–3242PubMedPubMedCentralCrossRef

30.

Deen B, Pitskel NB, Pelphrey KA (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 21(7):1498–1506PubMedCrossRef

31.

Dosenbach NUF, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RAT, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci U S A 104(26):11073–11078PubMedPubMedCentralCrossRef

32.

Bestelmeyer PEG, Pierre M, Julien R et al (2014) Adaptation to vocal expressions reveals multistep perception of auditory emotion. J Neurosci 34(24):8098–8105PubMedPubMedCentralCrossRef

33.

Craig ADB (2009) How do you feel--now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70PubMedCrossRef

34.

Mayberg HS (1997) Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatr Clin Neurosci 9(3):471–481CrossRef

35.

Palermo S, Morese R, Zibetti M, Dematteis F, Sirgiovanni S, Stanziano M, Valentini MC, Lopiano L (2017) Impulse control disorder and response-inhibition alterations in Parkinson’s disease. A rare case of totally absent functionality of the medial-prefrontal cortex and review of literature. J Adv Res 8(6):713–716PubMedPubMedCentralCrossRef

36.

Valerie B, Ham TE, Robert L et al (2012) Salience network integrity predicts default mode network function after traumatic brain injury. Proc Natl Acad Sci U S A 109(12):4690–4695CrossRef

37.

Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106(31):13040–13045PubMedPubMedCentralCrossRef

38.

van Tol MJ, Veer IM, van der Wee NJ et al (2013) Whole-brain functional connectivity during emotional word classification in medication-free major depressive disorder: abnormal salience circuitry and relations to positive emotionality. Neuroimage Clin 2:790–796PubMedPubMedCentralCrossRef

39.

Andrei M, Chun M, Felix B et al (2013) Insular dysfunction within the salience network is associated with severity of symptoms and aberrant inter-network connectivity in major depressive disorder. Front Hum Neurosci 7(2):930

40.

Dutta A, Mckie SDeakin JFW (2014) Resting state networks in major depressive disorder. Psychiatry Res 224(3):139–151PubMedCrossRef

41.

Trujillo JP, Gerrits NJ, Vriend C et al (2015) Impaired planning in Parkinson’s disease is reflected by reduced brain activation and connectivity. Hum Brain Mapp 36(9):3703–3715PubMedPubMedCentralCrossRef

42.

Bocquillon P, Bourriez JL, Palmero-Soler E, Defebvre L, Derambure P, Dujardin K (2015) Impaired early attentional processes in Parkinson’s disease: a high-resolution event-related potentials study. PLoS One 10(7):e0131654PubMedPubMedCentralCrossRef

43.

Phillips ML, Ladouceur CD, Drevets WC (2008) A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 13(9):829 833–57PubMedPubMedCentralCrossRef

44.

Chen T, Michels L, Supekar K, Kochalka J, Ryali S, Menon V (2015) Role of the anterior insular cortex in integrative causal signaling during multisensory auditory–visual attention. Eur J Neurosci 41(2):264–274PubMedCrossRef

45.

Eggers C, Pedrosa DJ, Kahraman D, Maier F, Lewis CJ, Fink GR, Schmidt M, Timmermann L (2012) Parkinson subtypes progress differently in clinical course and imaging pattern. PLoS One 7(10):e46813PubMedPubMedCentralCrossRef

46.

Nicoletti A, Mostile G, Nicoletti G, Arabia G, Iliceto G, Lamberti P, Marconi R, Morgante L, Barone P, Quattrone A, Zappia M (2016) Clinical phenotype and risk of levodopa-induced dyskinesia in Parkinson’s disease. J Neurol 263(5):888–894PubMedCrossRef

47.

Harrison MB, Wylie SA, Frysinger RC, Patrie JT, Huss DS, Currie LJ, Wooten GF (2009) UPDRS activity of daily living score as a marker of Parkinson’s disease progression. Mov Disord 24(2):224–230PubMedPubMedCentralCrossRef

48.

Smith R, Lane RD, Alkozei A, Bao J, Smith C, Sanova A, Nettles M, Killgore WDS (2017) Maintaining the feelings of others in working memory is associated with activation of the left anterior insula and left frontal-parietal control network. Soc Cogn Affect Neurosci 12(5):848–860PubMedPubMedCentralCrossRef

Titel: Different functional connectivity modes of the right fronto-insular cortex in akinetic-rigid and tremor-dominant Parkinson’s disease
verfasst von: Juan Wang
Yalian Shen
Juan Peng
Anran Wang
Xiaolin Wu
Xiaocui Chen
Jinjin Liu
Min Wei
Dezhi Zou
Yu Han
Oumei Cheng
Publikationsdatum: 24.11.2020
Verlag: Springer International Publishing
Erschienen in: Neurological Sciences / Ausgabe 7/2021
Print ISSN: 1590-1874
Elektronische ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-020-04917-1

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Different functional connectivity modes of the right fronto-insular cortex in akinetic-rigid and tremor-dominant Parkinson’s disease

Abstract

Background

Methods

Results

Conclusion

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Abstract

Background

Methods

Results

Conclusion

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