Skip to main content
Top
Published in: European Radiology 11/2019

01-11-2019 | Cough | Magnetic Resonance

Cortical morphology of chronic users of codeine-containing cough syrups: association with sulcal depth, gyrification, and cortical thickness

Authors: Meng Li, Kelei Hua, Shumei Li, Changhong Li, Wenfeng Zhan, Hua Wen, Xiaofen Ma, Junzhang Tian, Guihua Jiang

Published in: European Radiology | Issue 11/2019

Login to get access

Abstract

Objectives

The study aimed to explore the effects of codeine-containing cough syrup (CCS) exposure on cortical morphology and the relationship between cortical characteristics and CCS dependence.

Methods

Cortical morphometry based on Computational Anatomy Toolbox (CAT12) was used to compare changes in sulcal depth, gyrification, and cortical thickness of the cerebral cortex from 40 CCS users and 40 healthy controls (HCs) with two-sample t tests (p < 0.05, multiple comparison corrected). Relationships between abnormal cortical morphological changes and the duration of CCS use, impulsivity traits, and age of first use were investigated with correlation analysis (p < 0.05, uncorrected).

Results

CCS users exhibited significantly increased sulcal depth in the bilateral insula, bilateral lingual, bilateral superior frontal, right precuneus, and right middle frontal regions; increased gyrification in the right precentral cortex; and increased cortical thickness in the bilateral precentral, bilateral precuneus, and right superior temporal cortices compared to HCs. In addition, we found significant correlations between the bilateral insula, right superior frontal cortex, and right precentral gyrus and Barratt Impulsiveness Scale (BIS) total scores.

Conclusions

Chronic CCS abuse may be associated with aberrant sulcal depth, gyrification, and cortical thickness. These morphological changes might serve as an underlying neurobiological mechanism of impulsive behavior in the CCS users.

Key Points

• Cortical morphological changes were detected in CCS users.
• Increased sulcal depth, gyrification, and cortical thickness of some regions were found in the CCS users.
• Positive correlations between cortical morphological changes and BIS total scores were identified.
Literature
1.
go back to reference Hutchings HA, Eccles R (1994) The opioid agonist codeine and antagonist naltrexone do not affect voluntary suppression of capsaicin induced cough in healthy subjects. Eur Respir J 7:715–719CrossRefPubMed Hutchings HA, Eccles R (1994) The opioid agonist codeine and antagonist naltrexone do not affect voluntary suppression of capsaicin induced cough in healthy subjects. Eur Respir J 7:715–719CrossRefPubMed
2.
go back to reference Shek DT, Lam CM (2006) Adolescent cough medicine abuse in Hong Kong: implications for the design of positive youth development programs in Hong Kong. Int J Adolesc Med Health 18:493–503PubMed Shek DT, Lam CM (2006) Adolescent cough medicine abuse in Hong Kong: implications for the design of positive youth development programs in Hong Kong. Int J Adolesc Med Health 18:493–503PubMed
3.
go back to reference Vree TB, van Dongen RT, Koopman-Kimenai PM (2000) Codeine analgesia is due to codeine-6-glucuronide, not morphine. Int J Clin Pract 54:395–398PubMed Vree TB, van Dongen RT, Koopman-Kimenai PM (2000) Codeine analgesia is due to codeine-6-glucuronide, not morphine. Int J Clin Pract 54:395–398PubMed
4.
go back to reference Daumann J, Koester P, Becker B et al (2011) Medial prefrontal gray matter volume reductions in users of amphetamine-type stimulants revealed by combined tract-based spatial statistics and voxel-based morphometry. Neuroimage 54:794–801CrossRefPubMed Daumann J, Koester P, Becker B et al (2011) Medial prefrontal gray matter volume reductions in users of amphetamine-type stimulants revealed by combined tract-based spatial statistics and voxel-based morphometry. Neuroimage 54:794–801CrossRefPubMed
5.
go back to reference Brody AL, Mandelkern MA, Jarvik ME et al (2004) Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol Psychiatry 55:77–84CrossRefPubMed Brody AL, Mandelkern MA, Jarvik ME et al (2004) Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol Psychiatry 55:77–84CrossRefPubMed
6.
go back to reference Ersche KD, Jones PS, Williams GB, Turton AJ, Robbins TW, Bullmore ET (2012) Abnormal brain structure implicated in stimulant drug addiction. Science 335:601–604CrossRefPubMed Ersche KD, Jones PS, Williams GB, Turton AJ, Robbins TW, Bullmore ET (2012) Abnormal brain structure implicated in stimulant drug addiction. Science 335:601–604CrossRefPubMed
7.
go back to reference Ersche KD, Barnes A, Jones PS, Morein-Zamir S, Robbins TW, Bullmore ET (2011) Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence. Brain 134:2013–2024CrossRefPubMedPubMedCentral Ersche KD, Barnes A, Jones PS, Morein-Zamir S, Robbins TW, Bullmore ET (2011) Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence. Brain 134:2013–2024CrossRefPubMedPubMedCentral
8.
go back to reference Li M, Tian J, Zhang R et al (2014) Abnormal cortical thickness in heroin-dependent individuals. Neuroimage 88:295–307CrossRefPubMed Li M, Tian J, Zhang R et al (2014) Abnormal cortical thickness in heroin-dependent individuals. Neuroimage 88:295–307CrossRefPubMed
9.
go back to reference Meunier D, Ersche KD, Craig KJ et al (2012) Brain functional connectivity in stimulant drug dependence and obsessive-compulsive disorder. Neuroimage 59:1461–1468CrossRefPubMed Meunier D, Ersche KD, Craig KJ et al (2012) Brain functional connectivity in stimulant drug dependence and obsessive-compulsive disorder. Neuroimage 59:1461–1468CrossRefPubMed
10.
go back to reference Daglish MR, Weinstein A, Malizia AL et al (2003) Functional connectivity analysis of the neural circuits of opiate craving: “more” rather than “different”? Neuroimage 20:1964–1970CrossRefPubMed Daglish MR, Weinstein A, Malizia AL et al (2003) Functional connectivity analysis of the neural circuits of opiate craving: “more” rather than “different”? Neuroimage 20:1964–1970CrossRefPubMed
11.
go back to reference Qiu YW, Han LJ, Lv XF et al (2011) Regional homogeneity changes in heroin-dependent individuals: resting-state functional MR imaging study. Radiology 261:551–559CrossRefPubMed Qiu YW, Han LJ, Lv XF et al (2011) Regional homogeneity changes in heroin-dependent individuals: resting-state functional MR imaging study. Radiology 261:551–559CrossRefPubMed
12.
go back to reference Lopez-Larson MP, Bogorodzki P, Rogowska J et al (2011) Altered prefrontal and insular cortical thickness in adolescent marijuana users. Behav Brain Res 220:164–172CrossRefPubMedPubMedCentral Lopez-Larson MP, Bogorodzki P, Rogowska J et al (2011) Altered prefrontal and insular cortical thickness in adolescent marijuana users. Behav Brain Res 220:164–172CrossRefPubMedPubMedCentral
13.
go back to reference McQueeny T, Padula CB, Price J, Medina KL, Logan P, Tapert SF (2011) Gender effects on amygdala morphometry in adolescent marijuana users. Behav Brain Res 224:128–134CrossRefPubMedPubMedCentral McQueeny T, Padula CB, Price J, Medina KL, Logan P, Tapert SF (2011) Gender effects on amygdala morphometry in adolescent marijuana users. Behav Brain Res 224:128–134CrossRefPubMedPubMedCentral
14.
go back to reference Makris N, Gasic GP, Kennedy DN et al (2008) Cortical thickness abnormalities in cocaine addiction—a reflection of both drug use and a pre-existing disposition to drug abuse? Neuron 60:174–188CrossRefPubMedPubMedCentral Makris N, Gasic GP, Kennedy DN et al (2008) Cortical thickness abnormalities in cocaine addiction—a reflection of both drug use and a pre-existing disposition to drug abuse? Neuron 60:174–188CrossRefPubMedPubMedCentral
15.
go back to reference Moreno-López L, Catena A, Fernández-Serrano MJ et al (2012) Trait impulsivity and prefrontal gray matter reductions in cocaine dependent individuals. Drug Alcohol Depend 125:208–214CrossRefPubMed Moreno-López L, Catena A, Fernández-Serrano MJ et al (2012) Trait impulsivity and prefrontal gray matter reductions in cocaine dependent individuals. Drug Alcohol Depend 125:208–214CrossRefPubMed
16.
go back to reference Qiu YW, Su HH, Lv XF, Jiang GH (2015) Abnormal white matter integrity in chronic users of codeine-containing cough syrups: a tract-based spatial statistics study. AJNR Am J Neuroradiol 36:50–56CrossRefPubMed Qiu YW, Su HH, Lv XF, Jiang GH (2015) Abnormal white matter integrity in chronic users of codeine-containing cough syrups: a tract-based spatial statistics study. AJNR Am J Neuroradiol 36:50–56CrossRefPubMed
17.
go back to reference Hou H, Yin S, Jia S et al (2011) Decreased striatal dopamine transporters in codeine-containing cough syrup abusers. Drug Alcohol Depend 118:148–151CrossRefPubMed Hou H, Yin S, Jia S et al (2011) Decreased striatal dopamine transporters in codeine-containing cough syrup abusers. Drug Alcohol Depend 118:148–151CrossRefPubMed
18.
go back to reference Qiu YW, Lv XF, Jiang GH et al (2014) Reduced ventral medial prefrontal cortex (vmPFC) volume and impaired vmPFC-default mode network integration in codeine-containing cough syrups users. Drug Alcohol Depend 134:314–321CrossRefPubMed Qiu YW, Lv XF, Jiang GH et al (2014) Reduced ventral medial prefrontal cortex (vmPFC) volume and impaired vmPFC-default mode network integration in codeine-containing cough syrups users. Drug Alcohol Depend 134:314–321CrossRefPubMed
19.
go back to reference Lin HC, Wang PW, Wu HC, Ko CH, Yang YH, Yen CF (2018) Altered gray matter volume and disrupted functional connectivity of dorsolateral prefrontal cortex in men with heroin dependence. Psychiatry Clin Neurosci 72:435–444CrossRefPubMed Lin HC, Wang PW, Wu HC, Ko CH, Yang YH, Yen CF (2018) Altered gray matter volume and disrupted functional connectivity of dorsolateral prefrontal cortex in men with heroin dependence. Psychiatry Clin Neurosci 72:435–444CrossRefPubMed
20.
go back to reference Tamnes CK, Ostby Y, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2010) Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20:534–548CrossRefPubMed Tamnes CK, Ostby Y, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2010) Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20:534–548CrossRefPubMed
21.
go back to reference Gautam P, Anstey KJ, Wen W, Sachdev PS, Cherbuin N (2015) Cortical gyrification and its relationships with cortical volume, cortical thickness, and cognitive performance in healthy mid-life adults. Behav Brain Res 287:331–339CrossRefPubMed Gautam P, Anstey KJ, Wen W, Sachdev PS, Cherbuin N (2015) Cortical gyrification and its relationships with cortical volume, cortical thickness, and cognitive performance in healthy mid-life adults. Behav Brain Res 287:331–339CrossRefPubMed
22.
go back to reference Wei Q, Li M, Kang Z et al (2015) ZNF804A rs1344706 is associated with cortical thickness, surface area, and cortical volume of the unmedicated first episode schizophrenia and healthy controls. Am J Med Genet B Neuropsychiatr Genet 168B:265–273CrossRefPubMed Wei Q, Li M, Kang Z et al (2015) ZNF804A rs1344706 is associated with cortical thickness, surface area, and cortical volume of the unmedicated first episode schizophrenia and healthy controls. Am J Med Genet B Neuropsychiatr Genet 168B:265–273CrossRefPubMed
23.
go back to reference Pontious A, Kowalczyk T, Englund C, Hevner RF (2008) Role of intermediate progenitor cells in cerebral cortex development. Dev Neurosci 30:24–32CrossRefPubMed Pontious A, Kowalczyk T, Englund C, Hevner RF (2008) Role of intermediate progenitor cells in cerebral cortex development. Dev Neurosci 30:24–32CrossRefPubMed
24.
go back to reference Li Y, Yuan K, Cai C et al (2015) Reduced frontal cortical thickness and increased caudate volume within fronto-striatal circuits in young adult smokers. Drug Alcohol Depend 151:211–219CrossRefPubMed Li Y, Yuan K, Cai C et al (2015) Reduced frontal cortical thickness and increased caudate volume within fronto-striatal circuits in young adult smokers. Drug Alcohol Depend 151:211–219CrossRefPubMed
25.
go back to reference Kühn S, Schubert F, Gallinat J (2010) Reduced thickness of medial orbitofrontal cortex in smokers. Biol Psychiatry 68:1061–1065CrossRefPubMed Kühn S, Schubert F, Gallinat J (2010) Reduced thickness of medial orbitofrontal cortex in smokers. Biol Psychiatry 68:1061–1065CrossRefPubMed
26.
go back to reference Jacobus J, Squeglia LM, Sorg SF, Nguyen-Louie TT, Tapert SF (2014) Cortical thickness and neurocognition in adolescent marijuana and alcohol users following 28 days of monitored abstinence. J Stud Alcohol Drugs 75:729–743CrossRefPubMedPubMedCentral Jacobus J, Squeglia LM, Sorg SF, Nguyen-Louie TT, Tapert SF (2014) Cortical thickness and neurocognition in adolescent marijuana and alcohol users following 28 days of monitored abstinence. J Stud Alcohol Drugs 75:729–743CrossRefPubMedPubMedCentral
27.
go back to reference Migliorini R, Moore EM, Glass L et al (2015) Anterior cingulate cortex surface area relates to behavioral inhibition in adolescents with and without heavy prenatal alcohol exposure. Behav Brain Res 292:26–35CrossRefPubMedPubMedCentral Migliorini R, Moore EM, Glass L et al (2015) Anterior cingulate cortex surface area relates to behavioral inhibition in adolescents with and without heavy prenatal alcohol exposure. Behav Brain Res 292:26–35CrossRefPubMedPubMedCentral
28.
go back to reference Qiu YW, Lv XF, Jiang GH et al (2017) Potential gray matter unpruned in adolescents and young adults dependent on dextromethorphan-containing cough syrups: evidence from cortical and subcortical study. Brain Imaging Behav 11:1470–1478CrossRefPubMed Qiu YW, Lv XF, Jiang GH et al (2017) Potential gray matter unpruned in adolescents and young adults dependent on dextromethorphan-containing cough syrups: evidence from cortical and subcortical study. Brain Imaging Behav 11:1470–1478CrossRefPubMed
29.
go back to reference Im K, Lee JM, Yoon U et al (2006) Fractal dimension in human cortical surface: multiple regression analysis with cortical thickness, sulcal depth, and folding area. Hum Brain Mapp 27:994–1003CrossRefPubMed Im K, Lee JM, Yoon U et al (2006) Fractal dimension in human cortical surface: multiple regression analysis with cortical thickness, sulcal depth, and folding area. Hum Brain Mapp 27:994–1003CrossRefPubMed
30.
go back to reference Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM (2013) The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cereb Cortex 23:2521–2530CrossRefPubMed Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM (2013) The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cereb Cortex 23:2521–2530CrossRefPubMed
31.
go back to reference Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt Impulsiveness Scale. J Clin Psychol 51:768–774CrossRefPubMed Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt Impulsiveness Scale. J Clin Psychol 51:768–774CrossRefPubMed
32.
go back to reference Dahnke R, Yotter RA, Gaser C (2013) Cortical thickness and central surface estimation. Neuroimage 65:336–348CrossRefPubMed Dahnke R, Yotter RA, Gaser C (2013) Cortical thickness and central surface estimation. Neuroimage 65:336–348CrossRefPubMed
33.
go back to reference Luders E, Thompson PM, Narr KL, Toga AW, Jancke L, Gaser C (2006) A curvature-based approach to estimate local gyrification on the cortical surface. Neuroimage 29:1224–1230CrossRefPubMed Luders E, Thompson PM, Narr KL, Toga AW, Jancke L, Gaser C (2006) A curvature-based approach to estimate local gyrification on the cortical surface. Neuroimage 29:1224–1230CrossRefPubMed
34.
go back to reference Baler RD, Volkow ND (2006) Drug addiction: the neurobiology of disrupted self-control. Trends Mol Med 12:559–566CrossRefPubMed Baler RD, Volkow ND (2006) Drug addiction: the neurobiology of disrupted self-control. Trends Mol Med 12:559–566CrossRefPubMed
35.
go back to reference Asplund CL, Todd JJ, Snyder AP, Marois R (2010) A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention. Nat Neurosci 13:507–512CrossRefPubMedPubMedCentral Asplund CL, Todd JJ, Snyder AP, Marois R (2010) A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention. Nat Neurosci 13:507–512CrossRefPubMedPubMedCentral
36.
go back to reference Benoit RG, Gilbert SJ, Frith CD, Burgess PW (2012) Rostral prefrontal cortex and the focus of attention in prospective memory. Cereb Cortex 22:1876–1886CrossRefPubMed Benoit RG, Gilbert SJ, Frith CD, Burgess PW (2012) Rostral prefrontal cortex and the focus of attention in prospective memory. Cereb Cortex 22:1876–1886CrossRefPubMed
37.
go back to reference Walton ME, Devlin JT, Rushworth MF (2004) Interactions between decision making and performance monitoring within prefrontal cortex. Nat Neurosci 7:1259–1265CrossRef Walton ME, Devlin JT, Rushworth MF (2004) Interactions between decision making and performance monitoring within prefrontal cortex. Nat Neurosci 7:1259–1265CrossRef
38.
go back to reference Gläscher J, Adolphs R, Damasio H et al (2012) Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc Natl Acad Sci U S A 109:14681–14686CrossRefPubMed Gläscher J, Adolphs R, Damasio H et al (2012) Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc Natl Acad Sci U S A 109:14681–14686CrossRefPubMed
39.
go back to reference McNamee D, Rangel A, O’Doherty JP (2013) Category-dependent and category-independent goal-value codes in human ventromedial prefrontal cortex. Nat Neurosci 16:479–485CrossRefPubMed McNamee D, Rangel A, O’Doherty JP (2013) Category-dependent and category-independent goal-value codes in human ventromedial prefrontal cortex. Nat Neurosci 16:479–485CrossRefPubMed
40.
41.
go back to reference Crews FT, Braun CJ, Hoplight B, Switzer RC 3rd, Knapp DJ (2000) Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 24:1712–1723CrossRefPubMed Crews FT, Braun CJ, Hoplight B, Switzer RC 3rd, Knapp DJ (2000) Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 24:1712–1723CrossRefPubMed
43.
go back to reference Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237:1219–1223 Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237:1219–1223
44.
go back to reference Volkow ND, Fowler JS, Wang GJ (1999) Imaging studies on the role of dopamine in cocaine reinforcement and addiction in humans. J Psychopharmacol 13:337–345CrossRefPubMed Volkow ND, Fowler JS, Wang GJ (1999) Imaging studies on the role of dopamine in cocaine reinforcement and addiction in humans. J Psychopharmacol 13:337–345CrossRefPubMed
45.
go back to reference Gogtay N, Giedd JN, Lusk L et al (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101:8174–8179CrossRefPubMedPubMedCentral Gogtay N, Giedd JN, Lusk L et al (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101:8174–8179CrossRefPubMedPubMedCentral
46.
go back to reference Volkow ND, Fowler JS, Wang GJ, Goldstein RZ (2002) Role of dopamine, the frontal cortex and memory circuits in drug addiction: insight from imaging studies. Neurobiol Learn Mem 78:610–624CrossRefPubMed Volkow ND, Fowler JS, Wang GJ, Goldstein RZ (2002) Role of dopamine, the frontal cortex and memory circuits in drug addiction: insight from imaging studies. Neurobiol Learn Mem 78:610–624CrossRefPubMed
47.
go back to reference Tisserand DJ, Pruessner JC, Sanz Arigita EJ et al (2002) Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 17:657–669CrossRefPubMed Tisserand DJ, Pruessner JC, Sanz Arigita EJ et al (2002) Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 17:657–669CrossRefPubMed
48.
go back to reference Raz N, Lindenberger U, Rodrigue KM et al (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689CrossRefPubMed Raz N, Lindenberger U, Rodrigue KM et al (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689CrossRefPubMed
49.
go back to reference Sowell ER, Thompson PM, Tessner KD, Toga AW (2001) Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J Neurosci 21:8819–8829CrossRefPubMedPubMedCentral Sowell ER, Thompson PM, Tessner KD, Toga AW (2001) Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J Neurosci 21:8819–8829CrossRefPubMedPubMedCentral
50.
go back to reference Sowell ER, Thompson PM, Leonard CM, Welcome SE, Kan E, Toga AW (2004) Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 24:8223–8231CrossRefPubMedPubMedCentral Sowell ER, Thompson PM, Leonard CM, Welcome SE, Kan E, Toga AW (2004) Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 24:8223–8231CrossRefPubMedPubMedCentral
51.
go back to reference Volkow ND, Fowler JS, Wang GJ, Swanson JM (2004) Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Mol Psychiatry 9:557CrossRefPubMed Volkow ND, Fowler JS, Wang GJ, Swanson JM (2004) Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Mol Psychiatry 9:557CrossRefPubMed
53.
go back to reference Hester R, Nestor L, Garavan H (2009) Impaired error awareness and anterior cingulate cortex hypoactivity in chronic cannabis users. Neuropsychopharmacology 34:2450–2458CrossRefPubMedPubMedCentral Hester R, Nestor L, Garavan H (2009) Impaired error awareness and anterior cingulate cortex hypoactivity in chronic cannabis users. Neuropsychopharmacology 34:2450–2458CrossRefPubMedPubMedCentral
55.
go back to reference Clark L, Bechara A (2015) Commentary on Abdolahi et al (2015): Isolating the role of the insula in drug cravings. Addiction 110:2004–2005CrossRefPubMed Clark L, Bechara A (2015) Commentary on Abdolahi et al (2015): Isolating the role of the insula in drug cravings. Addiction 110:2004–2005CrossRefPubMed
57.
go back to reference Contreras M, Ceric F, Torrealba F (2007) Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318:655–658CrossRefPubMed Contreras M, Ceric F, Torrealba F (2007) Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318:655–658CrossRefPubMed
59.
go back to reference 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 105:12569–12574CrossRefPubMedPubMedCentral 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 105:12569–12574CrossRefPubMedPubMedCentral
60.
go back to reference Palaniyappan L, Liddle PF (2012) Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. J Psychiatry Neurosci 37:17–27CrossRefPubMedPubMedCentral Palaniyappan L, Liddle PF (2012) Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. J Psychiatry Neurosci 37:17–27CrossRefPubMedPubMedCentral
61.
go back to reference Naqvi NH, Bechara A (2010) The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making. Brain Struct Funct 214:435–450CrossRefPubMedPubMedCentral Naqvi NH, Bechara A (2010) The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making. Brain Struct Funct 214:435–450CrossRefPubMedPubMedCentral
62.
go back to reference Haldane M, Cunningham G, Androutsos C, Frangou S (2008) Structural brain correlates of response inhibition in bipolar disorder I. J Psychopharmacol 22:138–143CrossRefPubMed Haldane M, Cunningham G, Androutsos C, Frangou S (2008) Structural brain correlates of response inhibition in bipolar disorder I. J Psychopharmacol 22:138–143CrossRefPubMed
63.
go back to reference Jiang GH, Qiu YW, Zhang XL et al (2011) Amplitude low-frequency oscillation abnormalities in the heroin users: a resting state fMRI study. Neuroimage 57:149–154CrossRefPubMed Jiang GH, Qiu YW, Zhang XL et al (2011) Amplitude low-frequency oscillation abnormalities in the heroin users: a resting state fMRI study. Neuroimage 57:149–154CrossRefPubMed
64.
go back to reference Chang L, Yakupov R, Cloak C, Ernst T (2006) Marijuana use is associated with a reorganized visual-attention network and cerebellar hypoactivation. Brain 129:1096–1112CrossRefPubMed Chang L, Yakupov R, Cloak C, Ernst T (2006) Marijuana use is associated with a reorganized visual-attention network and cerebellar hypoactivation. Brain 129:1096–1112CrossRefPubMed
65.
go back to reference Im K, Lee JM, Seo SW, Kim SH, Kim SI, Na DL (2008) Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer’s disease. Neuroimage 43:103–113CrossRefPubMed Im K, Lee JM, Seo SW, Kim SH, Kim SI, Na DL (2008) Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer’s disease. Neuroimage 43:103–113CrossRefPubMed
66.
go back to reference Kochunov P, Mangin JF, Coyle T et al (2005) Age-related morphology trends of cortical sulci. Hum Brain Mapp 26:210–220CrossRefPubMed Kochunov P, Mangin JF, Coyle T et al (2005) Age-related morphology trends of cortical sulci. Hum Brain Mapp 26:210–220CrossRefPubMed
67.
go back to reference Kochunov P, Thompson PM, Coyle TR et al (2008) Relationship among neuroimaging indices of cerebral health during normal aging. Hum Brain Mapp 29:36–45CrossRefPubMed Kochunov P, Thompson PM, Coyle TR et al (2008) Relationship among neuroimaging indices of cerebral health during normal aging. Hum Brain Mapp 29:36–45CrossRefPubMed
68.
go back to reference Thatcher DL, Pajtek S, Chung T, Terwilliger RA, Clark DB (2010) Gender differences in the relationship between white matter organization and adolescent substance use disorders. Drug Alcohol Depend 110:55–61CrossRefPubMedPubMedCentral Thatcher DL, Pajtek S, Chung T, Terwilliger RA, Clark DB (2010) Gender differences in the relationship between white matter organization and adolescent substance use disorders. Drug Alcohol Depend 110:55–61CrossRefPubMedPubMedCentral
Metadata
Title
Cortical morphology of chronic users of codeine-containing cough syrups: association with sulcal depth, gyrification, and cortical thickness
Authors
Meng Li
Kelei Hua
Shumei Li
Changhong Li
Wenfeng Zhan
Hua Wen
Xiaofen Ma
Junzhang Tian
Guihua Jiang
Publication date
01-11-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 11/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-019-06165-0

Other articles of this Issue 11/2019

European Radiology 11/2019 Go to the issue