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Published in: Brain Structure and Function 8/2017

01-11-2017 | Original Article

Dysfunctions in striatal microstructure can enhance perceptual decision making through deficits in predictive coding

Authors: Christian Beste, Moritz Mückschel, Raymond Rosales, Aloysius Domingo, Lillian Lee, Arlene Ng, Christine Klein, Alexander Münchau

Published in: Brain Structure and Function | Issue 8/2017

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Abstract

An important brain function is to predict upcoming events on the basis of extracted regularities of previous inputs. These predictive coding processes can disturb performance in concurrent perceptual decision-making and are known to depend on fronto-striatal circuits. However, it is unknown whether, and if so, to what extent striatal microstructural properties modulate these processes. We addressed this question in a human disease model of striosomal dysfunction, i.e. X-linked dystonia-parkinsonism (XDP), using high-density EEG recordings and source localization. The results show faster and more accurate perceptual decision-making performance during distraction in XDP patients compared to healthy controls. The electrophysiological data show that sensory memory and predictive coding processes reflected by the mismatch negativity related to lateral prefrontal brain regions were weakened in XDP patients and thus induced less cognitive conflict than in controls as reflected by the N2 event-related potential (ERP). Consequently, attentional shifting (P3a ERP) and reorientation processes (RON ERP) were less pronounced in the XDP group. Taken together, these results suggests that striosomal dysfunction is related to predictive coding deficits leading to a better performance in concomitant perceptual decision-making, probably because predictive coding does not interfere with perceptual decision-making processes. These effects may reflect striatal imbalances between the striosomes and the matrix compartment.
Literature
go back to reference Berti S, Schröger E (2001) A comparison of auditory and visual distraction effects: behavioral and event-related indices. Brain Res Cogn Brain Res 10:265–273CrossRefPubMed Berti S, Schröger E (2001) A comparison of auditory and visual distraction effects: behavioral and event-related indices. Brain Res Cogn Brain Res 10:265–273CrossRefPubMed
go back to reference Beste C, Saft C, Güntürkün O, Falkenstein M (2008) Increased cognitive functioning in symptomatic Huntington’s disease as revealed by behavioral and event-related potential indices of auditory sensory memory and attention. J Neurosci 28:11695–11702. doi:10.1523/JNEUROSCI.2659-08.2008 CrossRefPubMed Beste C, Saft C, Güntürkün O, Falkenstein M (2008) Increased cognitive functioning in symptomatic Huntington’s disease as revealed by behavioral and event-related potential indices of auditory sensory memory and attention. J Neurosci 28:11695–11702. doi:10.​1523/​JNEUROSCI.​2659-08.​2008 CrossRefPubMed
go back to reference Beste C, Stock A-K, Ness V et al (2015) Evidence for divergent effects of neurodegeneration in Huntington’s disease on attentional selection and neural plasticity: implications for excitotoxicity. Brain Struct Funct 220:1437–1447. doi:10.1007/s00429-014-0735-7 CrossRefPubMed Beste C, Stock A-K, Ness V et al (2015) Evidence for divergent effects of neurodegeneration in Huntington’s disease on attentional selection and neural plasticity: implications for excitotoxicity. Brain Struct Funct 220:1437–1447. doi:10.​1007/​s00429-014-0735-7 CrossRefPubMed
go back to reference Beste C, Mückschel M, Rosales R et al (2017) Striosomal dysfunction affects behavioral adaptation but not impulsivity—evidence from X-linked dystonia-parkinsonism. Mov Disord. doi:10.1002/mds.26895 PubMed Beste C, Mückschel M, Rosales R et al (2017) Striosomal dysfunction affects behavioral adaptation but not impulsivity—evidence from X-linked dystonia-parkinsonism. Mov Disord. doi:10.​1002/​mds.​26895 PubMed
go back to reference Eblen F, Graybiel AM (1995) Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J Neurosci 15:5999–6013PubMed Eblen F, Graybiel AM (1995) Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J Neurosci 15:5999–6013PubMed
go back to reference Gerfen CR (1989) The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246:385–388CrossRefPubMed Gerfen CR (1989) The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246:385–388CrossRefPubMed
go back to reference Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC (1996) Role of cortical N-methyl-d-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci USA 93:11962–11967CrossRefPubMedPubMedCentral Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC (1996) Role of cortical N-methyl-d-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci USA 93:11962–11967CrossRefPubMedPubMedCentral
go back to reference Kreitschmann-Andermahr I, Rosburg T, Demme U et al (2001) Effect of ketamine on the neuromagnetic mismatch field in healthy humans. Brain Res Cogn Brain Res 12:109–116CrossRefPubMed Kreitschmann-Andermahr I, Rosburg T, Demme U et al (2001) Effect of ketamine on the neuromagnetic mismatch field in healthy humans. Brain Res Cogn Brain Res 12:109–116CrossRefPubMed
go back to reference Lee LV, Kupke KG, Caballar-Gonzaga F et al (1991) The phenotype of the X-linked dystonia-parkinsonism syndrome. An assessment of 42 cases in the Philippines. Medicine (Baltimore) 70:179–187CrossRef Lee LV, Kupke KG, Caballar-Gonzaga F et al (1991) The phenotype of the X-linked dystonia-parkinsonism syndrome. An assessment of 42 cases in the Philippines. Medicine (Baltimore) 70:179–187CrossRef
go back to reference Martin LJ, Blackstone CD, Huganir RL, Price DL (1993) The striatal mosaic in primates: striosomes and matrix are differentially enriched in ionotropic glutamate receptor subunits. J Neurosci 13:782–792PubMed Martin LJ, Blackstone CD, Huganir RL, Price DL (1993) The striatal mosaic in primates: striosomes and matrix are differentially enriched in ionotropic glutamate receptor subunits. J Neurosci 13:782–792PubMed
go back to reference Miura M, Saino-Saito S, Masuda M et al (2007) Compartment-specific modulation of GABAergic synaptic transmission by mu-opioid receptor in the mouse striatum with green fluorescent protein-expressing dopamine islands. J Neurosci 27:9721–9728. doi:10.1523/JNEUROSCI.2993-07.2007 CrossRefPubMed Miura M, Saino-Saito S, Masuda M et al (2007) Compartment-specific modulation of GABAergic synaptic transmission by mu-opioid receptor in the mouse striatum with green fluorescent protein-expressing dopamine islands. J Neurosci 27:9721–9728. doi:10.​1523/​JNEUROSCI.​2993-07.​2007 CrossRefPubMed
go back to reference Mückschel M, Stock A-K, Beste A-C (2014) Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cereb Cortex N Y N 1991 24:2120–2129. doi:10.1093/cercor/bht066 Mückschel M, Stock A-K, Beste A-C (2014) Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cereb Cortex N Y N 1991 24:2120–2129. doi:10.​1093/​cercor/​bht066
go back to reference Näätänen R, Winkler I (1999) The concept of auditory stimulus representation in cognitive neuroscience. Psychol Bull 125:826–859CrossRefPubMed Näätänen R, Winkler I (1999) The concept of auditory stimulus representation in cognitive neuroscience. Psychol Bull 125:826–859CrossRefPubMed
go back to reference Nunez PL, Pilgreen KL (1991) The spline-Laplacian in clinical neurophysiology: a method to improve EEG spatial resolution. J Clin Neurophysiol 8:397–413CrossRefPubMed Nunez PL, Pilgreen KL (1991) The spline-Laplacian in clinical neurophysiology: a method to improve EEG spatial resolution. J Clin Neurophysiol 8:397–413CrossRefPubMed
go back to reference Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24 Suppl D:5–12PubMed Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24 Suppl D:5–12PubMed
go back to reference Prensa L, Parent A (2001) The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247–7260PubMed Prensa L, Parent A (2001) The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247–7260PubMed
go back to reference Schröger E, Wolff C (1998) Behavioral and electrophysiological effects of task-irrelevant sound change: a new distraction paradigm. Brain Res Cogn Brain Res 7:71–87CrossRefPubMed Schröger E, Wolff C (1998) Behavioral and electrophysiological effects of task-irrelevant sound change: a new distraction paradigm. Brain Res Cogn Brain Res 7:71–87CrossRefPubMed
go back to reference Schröger E, Giard MH, Wolff C (2000) Auditory distraction: event-related potential and behavioral indices. Clin Neurophysiol 111:1450–1460CrossRefPubMed Schröger E, Giard MH, Wolff C (2000) Auditory distraction: event-related potential and behavioral indices. Clin Neurophysiol 111:1450–1460CrossRefPubMed
go back to reference Umbricht D, Koller R, Vollenweider FX, Schmid L (2002) Mismatch negativity predicts psychotic experiences induced by NMDA receptor antagonist in healthy volunteers. Biol Psychiatry 51:400–406CrossRefPubMed Umbricht D, Koller R, Vollenweider FX, Schmid L (2002) Mismatch negativity predicts psychotic experiences induced by NMDA receptor antagonist in healthy volunteers. Biol Psychiatry 51:400–406CrossRefPubMed
Metadata
Title
Dysfunctions in striatal microstructure can enhance perceptual decision making through deficits in predictive coding
Authors
Christian Beste
Moritz Mückschel
Raymond Rosales
Aloysius Domingo
Lillian Lee
Arlene Ng
Christine Klein
Alexander Münchau
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 8/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1435-x

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