Abstract
Neuropsychological studies have shown that alcohol dependence is associated with neurocognitive deficits in tasks requiring memory, perceptual motor skills, abstraction and problem solving, whereas language skills are relatively spared in alcoholics despite structural abnormalities in the language-related brain regions. To investigate the preserved mechanisms of language processing in alcohol-dependents, functional brain imaging was undertaken in healthy controls (n=18) and alcohol-dependents (n=16) while completing a lexical semantic judgment task in a 3 T MR scanner. Behavioural data indicated that alcohol-dependents took more time than controls for performing the task but there was no significant difference in their response accuracy. fMRI data analysis revealed that while performing the task, the alcoholics showed enhanced activations in left supramarginal gyrus, precuneus bilaterally, left angular gyrus, and left middle temporal gyrus as compared to control subjects. The extensive activations observed in alcoholics as compared to controls suggest that alcoholics recruit additional brain areas to meet the behavioural demands for equivalent task performance. The results are consistent with previous fMRI studies suggesting compensatory mechanisms for the execution of task for showing an equivalent performance or decreased neural efficiency of relevant brain networks. However, on direct comparison of the two groups, the results did not survive correction for multiple comparisons; therefore, the present findings need further exploration.
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Andoh J, Artiges E, Pallier C, Riviere D, Mangin JF and Cachia A 2006 Modulation of language areas with functional MR image-guided magnetic stimulation. Neuroimage 29 619–627
Andoh J, Artiges E, Pallier C, Riviere D, Mangin JF and Paillere-Martinot ML 2007 Priming frequencies of transcranial magnetic stimulation over Wernicke’s area modulate word detection. Cereb. Cortex 18 210–216
Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM and Prieto T 1997 Human brain language areas identified by functional magnetic resonance imaging. J. Neurosci. 17 353–362
Binder JR, Swanson SJ, Hammeke TA, Morris GL, Mueller WM and Fischer M 1996 Determination of language dominance using functional MRI: a comparison with the Wada test. Neurology 46 978–984
Bitan T, Booth JR, Choy J, Burman DR, Gitelman DR and Mesulam MM 2005 Shifts in effective connectivity within a language network during rhyming and spelling. J. Neurosci. 25 5397–5403
Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, Fotenos AF, Sheline YI, Klunk WE, et al. 2005 Molecular, structural, and functional characterization of Alzheimer’s disease: Evidence for a relationship between default activity, amyloid, and memory. J. Neurosci. 25 7709–7717
Burnstine TH, Lesser RP, Hart J, Luematsu S, Zinreich S and Krauss GL 1990 Characterization of the basal temporal language area in patients with left temporal lobe epilepsy. Neurology 40 966–970
Campanella S, Peigneux P, Petit G, Lallemand F, Saeremans M, Noël X, Metens T, Nouali M, et al. 2013 Increased cortical activity in binge drinkers during working memory task: a preliminary assessment through a functional magnetic resonance imaging study. PLoS One 8 e62260
Cappa S, Cavallotti G and Vignolo LA 1981 Phonemic and lexical errors in fluent aphasia: correlation with lesion site. Neuropsychologia 19 171–7
Catani M and Ffytche DH 2005 The rises and falls of disconnection syndromes. Brain 128 2224–2239
Chanraud S, Andoh J, Martelli C,Artiges E,Pallier C, Aubin HJ, Martinot JL, Reynauld M 2009 Imaging of language-related brain regions in detoxified alcoholics. Alcohol Clin. Exp. Res. 33 6–8
Chanraud S, Martelli C, Delain F, Kostogianni N, Douaud G, Aubin HJ, Reynaud M and Martinot JL 2007 Brain morphometry and cognitive performance in detoxified alcohol-dependents with preserved psychosocial functioning. Neuropsychopharmacology 32 429–438
Chee M, Hon N, Lee HL and Soon CS 2001 Relative language proficiency modulates BOLD signal change when bilinguals perform semantic judgments. Neuroimage 13 1155–1163
Chertkow H, Bub D, Deaudon C and Whitehead V 1997 On the status of object concepts in aphasia. Brain Lang. 58 203–232
Christoff K, Prabhakaran V, Dorfman J, Zhao Z, Kroger JK and Holyoak K J 2001 Rostrolateral prefrontal cortex involvement in relational integration during reasoning. Neuroimage 14 1136–1149
Crews FT, Buckley T, Dodd PR, Ende G, Foley N, Harper C, He J, Innes D, Loh el-W, Pfefferbaum A, Zou J and Sullivan EV 2005 Alcoholic neurobiology: changes in dependence and recovery. Alcohol Clin. Exp. Res. 29 1504–1513
Crews FT and Nixon K 2009 Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol. 44 115–127
Damasio H, Grabowski TJ, Tranel D, Hichwa RD and Damasio AR 1996 A neural basis for lexical retrieval. Nature 380 499–505
Das T, Padakannaya P, Pugh KR and Singh NC 2011 Neuroimaging reveals dual routes to reading in simultaneous proficient readers of two orthographies. Neuroimage 54 1476–1487
Demirakca T, Ende G, Kammerer N, Welzel-Marquez H, Hermann D, Heinz A and Mann K 2011 Effects of alcoholism and continued abstinence on brain volumes in both genders. Alcohol Clin. Exp. Res. 35 1678–1685
Demonet JF, Chollet F, Ramsay S, Cardebat D, Nespoulous JL and Wise R 1992 The anatomy of phonological and semantic processing in normal subjects. Brain 115 1753–1768
Di Virgilio G and Clarke S 1997 Direct interhemispheric visual input to human speech areas. Hum. Brain Map. 5 347–354
Duka T, Townshend JM, Collier K and Stephens DN 2003 Impairment in cognitive functions after multiple detoxifications in alcoholic inpatients. Alcohol Clin. Exp. Res. 27 1563–1572
Eickhoff S, Stephan KE, Mohlberg H, Grefkes C, Fink GR and Amunts K 2005 A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25 1325–1335
Elizabeth J, Karalyn P, Roy WJ, Matthew A and Lambon R 2009 Comprehension of concrete and abstract words in semantic dementia. Neuropsychology 23 492–99
Fabian MS, Parsons OA and Sheldon MD 1994 Effects of gender and alcoholism on verbal and visuospatial learning. J. Nerv. Ment. Dis. 172 16–20
First MB, Spitzer RL, Miriam G and Williams JBW 2007 Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition (SCID-I/P) (New York: New York State Psychiatric Institute)
Folstein MF, Folstein SE and McHugh PR 1975 Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12 189–198
Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA and Noll DC 1995 Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magn. Reson. Med. 33 636–647
Foundas AL, Daniels SK and Vasterling JJ 1998 Anomia: case studies with lesion localisation. Neurocase 4 35–43
Friston KJ and Worksley KJ 1995 Analysis of fMRI time series revisited again. Neuroimage 2 173–181
Gabrieli JE, Desmond JE, Demb JB and Wagner AD 1996 Functional magnetic resonance imaging of semantic memory processes in the frontal lobes. Psychol. Sci. 7 278–283
Geschwind N 1965 Disconnexion syndromes in animals and man. II. Brain 88 585–644
Gilman JM, Davis MB and Hommer DW 2010 Greater activation in left hemisphere language-related regions during simple judgment tasks among substance-dependent patients in treatment for alcoholism. Alcohol Clin. Exp. Res. 34 331–341
Grossman M, Payer F, Onishi K, Devine TW, Morrison D and D'Esposito M 1997 Constraints on the cerebral basis for semantic processing from neuroimaging studies of Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 63 152–158
Kim KK, Karunanayaka P, Privitera MD, Holland SK and Szaflarski JP 2011 Semantic association investigated with fMRI and independent component analysis. Epilepsy Behav. 20 613–622
Kiyosawa M, Inoue C, Kawasaki T, Tokoro T, Ishii K and Ohyama M 1996 Functional neuroanatomy of visual object naming: a PET study. Graefes Arch. Clin. Exp. Ophthalmol. 234 110–115
Klostermann EC, Kane AJ and Shimamura AP 2008 Parietal activation during retrieval of abstract and concrete auditory information. Neuroimage 40 896–901
Kosslyn SM, Alpert NM, Thompson WL, Maljkovic V, Weise SB and Chabris CF 1993 Visual mental imagery activates topographically organized visual cortex: PET investigations. J. Cogn. Neurosci. 5 263–287
Kroger JK, Sabb FW, Fales CL, Bookheimer SY, Cohen MS and Holyoak KJ 2002 Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity. Cereb. Cortex 12 477–485
Lee KH, Choi YY, Gray JR, Cho SH, Chae JH and Lee S 2006 Neural correlates of superior intelligence: stronger recruitment of posterior parietal cortex. Neuroimage 29 578–586
Lundstrom BN, Martin Ingvar M and Petersson KM 2005 The role of precuneus and left inferior frontal cortex during source memory episodic retrieval. Neuroimage 27 824–834
Malogiannis IA, Valaki C, Smyrnis N, Papathanasiou M, Evdokimidis I and Baras P 2003 Functional magnetic resonance imaging (fMRI) during a language comprehension task. J. Neurolinguistics 16 407–416
Marian V, Blumenfeld HK and Kaushanskaya M 2007 The Language Experience and Proficiency Questionnaire (LEAP-Q): Assessing language profiles in bilinguals and multilinguals. J. Speech Lang. Hear Res. 50 940–967
Marinkovic K, Dhond RP, Dale AM, Glessner M, Carr V and Halgren E 2003 Spatiotemporal dynamics of modality-specific and supramodal word processing. Neuron 38 487–497
Matthew KL, Timothy TB, Katherine ET, Lusineh G, Donald JH and Anders MD 2010 Spatiotemporal dynamics of bilingual word processing. Neuroimage 49 3286–3294
Mummery CJ, Patterson K, Wise RJS, Vandenbergh R, Price CJ and Hodges JR 1999 Disrupted temporal lobe connections in semantic dementia. Brain 122 61–73
Nahor A and Benson DF 1970 A screening test for organic brain disease in emergency psychiatric evaluation. Behav. Neuropsych. 2 23–26
Oscar-Berman M and Marinkovic K 2003 Alcoholism and the brain: An overview. Alcohol Res. Health 27 125–133
Pallier C, Dehaene S, Poline JB, LeBihan D, Argenti AM and Dupoux E 2003 Brain imaging of language plasticity in adopted adults: can a second language replace the first? Cereb. Cortex 13 155–161
Parsons OA 1998 Neurocognitive deficits in alcoholics and social drinkers: a continuum? Alcohol Clin. Exp. Res. 22 954–961
Pershad D and Verma SK 1990 Handbook of PGI battery of brain dysfunction (PGI-BBD) (Agra, India: National Psychological Corporation)
Pfefferbaum A, Desmond JE, Galloway C, Menon V, Glover GH and Sullivan EV 2001 Reorganization of frontal systems used by alcoholics for spatial working memory: An fMRI study. Neuroimage 14 7–20
Poldrack RA, Wagner AD, Prull MW, Desmond JE, Glover GH and Gabrieli JD 1999 Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage 10 15–35
Prabhakaran V, Smith JA, Desmond JE, Glover GH and Gabrieli JD 1997 Neural substrates of fluid reasoning: An fMRI study of neocortical activation during performance of the Raven’s Progressive Matrices Test. Cogn. Psychol. 33 43–63
Price CJ and Friston KJ 1997 Cognitive conjunction: a new approach to brain activation experiments. Neuroimage 5 261–270
Sahu RN, Naik GP, Dusad A and Agrawal VK 2005 Neurocognitive function in women affected by the Bhopal gas disaster. Indian J. Psychiatry 47 51–53
Seghier ML, Lazeyras F, Pegna AJ, Annoni JM, Zimine I and Mayer E 2004 A Variability of fMRI activation during a phonological and semantic language task in healthy subjects. Hum. Brain Map. 23 140–155
Stavro K, Pelletier J and Potvin S 2013 Widespread and sustained cognitive deficits in alcoholism: a meta-analysis. Addict. Biol. 18 203–213
Sullivan EV, Harding AJ, Pentney R, Dlugos C, Martin PR and Parks MH 2003 A Disruption of frontocerebellar circuitry and function in alcoholism. Alcohol Clin. Exp. Res. 27 301–309
Sullivan EV, Deshmukh A, Desmond JE, Lim KO and Pfefferbaum A 2000 Cerebellar volume decline in normal aging, alcoholism, and Korsakoff’s syndrome: relation to ataxia. Neuropsychology 14 341–352
Sullivan EV 2003 Compromised pontocerebellar and cerebellothalamocortical systems: speculations on their contributions to cognitive and motor impairment in nonamnesic alcoholism. Alcohol Clin. Exp. Res. 27 1409–1419
Vogt BA and Laureys S 2005 Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog. Brain Res. 150 205–17
Warrington EK and Shallice TIM 1979 Semantic access dyslexia. Brain 102 43–63
Wegner AJ, Gunthner A and Fahle M 2001 Visual performance and recovery in recently detoxified alcoholics. Alcohol Alcohol. 36 171–179
Wig NN, Pershad D and Verma SK 1983 C.M.I. Health Questionnaire (Agra: Psychological Corporation)
Acknowledgements
This work was supported by DRDO R&D Project No. INM 311 (4.1) and Council of scientific and Industrial Research (CSIR), India. None of the authors has any conflict of interest to declare.
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Corresponding editor: NEERAJ JAIN
MS received 06 February 2013; accepted 25 September 2013
Corresponding editor: Neeraj Jain
[Bagga D, Singh N, Modi S, Kumar P, Bhattacharya D, Garg ML and Khushu S 2013 Assessment of lexical semantic judgment abilities in alcohol-dependent subjects: An fMRI study. J. Biosci. 38 1–11] DOI 10.1007/s12038-013-9387-7
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Bagga, D., Singh, N., Modi, S. et al. Assessment of lexical semantic judgment abilities in alcohol-dependent subjects: An fMRI study. J Biosci 38, 905–915 (2013). https://doi.org/10.1007/s12038-013-9387-7
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DOI: https://doi.org/10.1007/s12038-013-9387-7