Spatial frequency processing and its modulation by emotional content in severe alcohol use disorder.
Alcohol use disorder
Emotion
Faces
Magnocellular
Parvocellular
Spatial frequency
Vision
Visual pathways
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
Aug 2022
Aug 2022
Historique:
received:
16
12
2021
accepted:
27
04
2022
pubmed:
7
5
2022
medline:
22
7
2022
entrez:
6
5
2022
Statut:
ppublish
Résumé
Visuo-perceptive deficits in severe alcohol use disorder (SAUD) remain little understood, notably regarding the respective involvement of the two main human visual streams, i.e., magnocellular (MC) and parvocellular (PC) pathways, in these deficits. Besides, in healthy populations, low-level visual perception can adapt depending on the nature of visual cues, among which emotional features, but this MC and PC pathway adaptation to emotional content is unexplored in SAUD. To assess MC and PC functioning as well as their emotional modulations in SAUD. We used sensitivity indices (d') and repeated-measures analyses of variance to compare orientation judgments of Gabor patches sampled at various MC- and PC-related spatial frequencies in 35 individuals with SAUD and 38 matched healthy controls. We then explored how emotional content modulated performances by introducing neutral or fearful face cues immediately before the Gabor patches and added the type of cue in the analyses. SAUD patients showed a general reduction in sensitivity across all spatial frequencies, indicating impoverished processing of both coarse and fine-scale visual content. However, we observed selective impairments depending on facial cues: individuals with SAUD processed intermediate spatial frequencies less efficiently than healthy controls following neutral faces, whereas group differences emerged for the highest spatial frequencies following fearful faces. Altogether, SAUD was associated with mixed MC and PC deficits that may vary according to emotional content, in line with a flexible but suboptimal use of low-level visual content. Such subtle alterations could have implications for everyday life's complex visual judgments.
Identifiants
pubmed: 35524008
doi: 10.1007/s00213-022-06158-w
pii: 10.1007/s00213-022-06158-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2647-2657Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders (5th ed.). https://doi.org/10.1176/appi.books.9780890425596
Andre JT (1996) Visual functioning in challenging conditions: effects of alcohol consumption, luminance, stimulus motion, and glare on contrast sensitivity. J Exp Psychol Appl 2:250–269. https://doi.org/10.1037/1076-898X.2.3.250
doi: 10.1037/1076-898X.2.3.250
Babor TF, Higgins-Biddle JC, Saunders JB, Monteiro MG (2001) AUDIT: the Alcohol Use Disorders Identification Test: guidelines for use in primary health care, 2nd edn. World Health Organization, Geneva
Bach M (1996) The Freiburg Visual Acuity test — automatic measurement of visual acuity. Optom vis Sci 73:49–53. https://doi.org/10.1097/00006324-199601000-00008
doi: 10.1097/00006324-199601000-00008
pubmed: 8867682
Bach M (2007) The Freiburg Visual Acuity Test-variability unchanged by post-hoc re-analysis. Graefes Arch Clin Exp Ophthalmol 245:965–971. https://doi.org/10.1007/s00417-006-0474-4
doi: 10.1007/s00417-006-0474-4
pubmed: 17219125
Bagga D, Sharma A, Kumari A et al (2014) Decreased white matter integrity in fronto-occipital fasciculus bundles: relation to visual information processing in alcohol-dependent subjects. Alcohol 48:43–53. https://doi.org/10.1016/j.alcohol.2013.10.009
doi: 10.1016/j.alcohol.2013.10.009
pubmed: 24388377
Bar M (2004) Visual objects in context. Nat Rev Neurosci 5:617–629. https://doi.org/10.1038/nrn1476
doi: 10.1038/nrn1476
pubmed: 15263892
Beck AT, Steer RA, Brown GK (1996) BDI-II: Beck Depression Inventory Manual., 2nd edn. Psychological Corporation, San Antonio, TX
Bocanegra BR, Zeelenberg R (2009) Emotion improves and impairs early vision. Psychol Sci 20:707–713. https://doi.org/10.1111/j.1467-9280.2009.02354.x
doi: 10.1111/j.1467-9280.2009.02354.x
pubmed: 19422624
Bora E, Zorlu N (2017) Social cognition in alcohol use disorder: a meta-analysis. Addiction 112:40–48. https://doi.org/10.1111/add.13486
doi: 10.1111/add.13486
pubmed: 27287050
Braun CM, Richer M (1993) A comparison of functional indexes, derived from screening tests, of chronic alcoholic neurotoxicity in the cerebral cortex, retina and peripheral nervous system. J Stud Alcohol 54:11–16. https://doi.org/10.15288/jsa.1993.54.11
doi: 10.15288/jsa.1993.54.11
pubmed: 8355495
Campbell FW, Robson JG (1968) Application of fourier analysis to the visibility of gratings. J Physiol 197:551–566. https://doi.org/10.1113/jphysiol.1968.sp008574
doi: 10.1113/jphysiol.1968.sp008574
pubmed: 5666169
pmcid: 1351748
Caplette L, West G, Gomot M et al (2014) Affective and contextual values modulate spatial frequency use in object recognition. Front Psychol 5:512. https://doi.org/10.3389/fpsyg.2014.00512
doi: 10.3389/fpsyg.2014.00512
pubmed: 24904514
pmcid: 4036062
Casares-López M, Castro-Torres JJ, Martino F et al (2020) Contrast sensitivity and retinal straylight after alcohol consumption: effects on driving performance. Sci Rep 10:13599. https://doi.org/10.1038/s41598-020-70645-3
doi: 10.1038/s41598-020-70645-3
pubmed: 32788613
pmcid: 7423611
Cavalcanti-Galdino MK, da Silva JA, Mendes LC et al (2014) Acute effect of alcohol intake on sine-wave Cartesian and polar contrast sensitivity functions. Braz J Med Biol Res 47:321–327. https://doi.org/10.1590/1414-431X20143209
doi: 10.1590/1414-431X20143209
pubmed: 24676473
pmcid: 4075296
Chambers JL, Wilson WT (1968) Perception of apparent motion and degree of mental pathology. Percept Mot Skills 26:855–861. https://doi.org/10.2466/pms.1968.26.3.855
doi: 10.2466/pms.1968.26.3.855
pubmed: 5657736
Collin CA, Therrien M, Martin C, Rainville S (2006) Spatial frequency thresholds for face recognition when comparison faces are filtered and unfiltered. Percept Psychophys 68:879–889. https://doi.org/10.3758/BF03193351
doi: 10.3758/BF03193351
pubmed: 17153184
Creupelandt C, D’Hondt F, Bocanegra B, et al (2022) Visual abilities in Severe Alcohol Use Disorder: Preserved spatial but impaired temporal resolution. J Psychiat Res 149:201–208. https://doi.org/10.1016/j.jpsychires.2022.02.040
Creupelandt C, D’Hondt F, Maurage P (2021a) Neural correlates of visuoperceptive changes in severe alcohol use disorder: a critical review of neuroimaging and electrophysiological findings. J Neurosci Res 99:1253–1275. https://doi.org/10.1002/jnr.24799
doi: 10.1002/jnr.24799
pubmed: 33550638
Creupelandt C, Maurage P, D’Hondt F (2021) Visuoperceptive impairments in severe alcohol use disorder: a critical review of behavioral studies. Neuropsychol Rev 31:361–384. https://doi.org/10.1007/s11065-020-09469-x
doi: 10.1007/s11065-020-09469-x
pubmed: 33591477
Creupelandt C, Maurage P, Lenoble Q et al (2021) Magnocellular and parvocellular mediated luminance contrast discrimination in severe alcohol use disorder. Alcohol Clin Exp Res 45:375–385. https://doi.org/10.1111/acer.14541
doi: 10.1111/acer.14541
pubmed: 33349930
Cruz ÉDN da, Andrade MJO de, Cavalcanti-Gaudino MK et al (2016) Effects of chronic alcoholism in the sensitivity to luminance contrast in vertical sinusoidal gratings. Psicologia: Reflexão e Crítica 29. https://doi.org/10.1186/s41155-016-0023-y
Demmin DL, Fradkin SI, Silverstein SM (2019) Remediation of visual processing impairments in schizophrenia: where we are and where we need to be. Curr Behav Neurosci Rep 6:13–20. https://doi.org/10.1007/s40473-019-00171-8
doi: 10.1007/s40473-019-00171-8
de Oliveira Castro AJ, Rodrigues AR, Côrtes MIT, de Lima Silveira LC (2009) Impairment of color spatial vision in chronic alcoholism measured by psychophysical methods. Psychol Neurosci 2:179–187. https://doi.org/10.3922/j.psns.2009.2.009
doi: 10.3922/j.psns.2009.2.009
De Valois RL, Cottaris NP, Mahon LE et al (2000) Spatial and temporal receptive fields of geniculate and cortical cells and directional selectivity. Vision Res 40:3685–3702. https://doi.org/10.1016/S0042-6989(00)00210-8
doi: 10.1016/S0042-6989(00)00210-8
pubmed: 11090662
De Valois RL, De Valois KK (1988) Spatial vision. Oxford University Press, New York
Dosher B, Lu Z-L (2017) Visual perceptual learning and models. Annu Rev vis Sci 3:343–363. https://doi.org/10.1146/annurev-vision-102016-061249
doi: 10.1146/annurev-vision-102016-061249
pubmed: 28723311
pmcid: 6691499
Ekman P, Hager JC, Friesen WV (2002) Facial action coding system: the manual. Research Nexus, Salt Lake City
Fein G, Shimotsu R, Chu R, Barakos J (2009) Parietal gray matter volume loss is related to spatial processing deficits in long-term abstinent alcoholic men. Alcohol Clin Exp Res 33:1806–1814. https://doi.org/10.1111/j.1530-0277.2009.01019.x
doi: 10.1111/j.1530-0277.2009.01019.x
pubmed: 19645730
pmcid: 2755629
Ferneyhough E, Stanley DA, Phelps EA, Carrasco M (2010) Cuing effects of faces are dependent on handedness and visual field. Psychon Bull Rev 17:529–535. https://doi.org/10.3758/PBR.17.4.529
doi: 10.3758/PBR.17.4.529
pubmed: 20702873
pmcid: 3150162
Goldstein EB (2010) Sensation and perception, 8th edn. Wadsworth, Cengage Learning, Belmont, California
Hartung B, Schwender H, Ritz-Timme S et al (2020) Ophthalmologic examinations under the acute influence of alcohol. Leg Med 46:101722. https://doi.org/10.1016/j.legalmed.2020.101722
doi: 10.1016/j.legalmed.2020.101722
Hoffman LA, Lewis B, Nixon SJ (2019) Neurophysiological and interpersonal correlates of emotional face processing in alcohol use disorder. Alcohol Clin Exp Res 43:1928–1936. https://doi.org/10.1111/acer.14152
doi: 10.1111/acer.14152
pubmed: 31403716
pmcid: 6934372
Kapitany T, Dietzel M, Grunberger J et al (1993) Color vision deficiencies in the course of acute alcohol withdrawal. Biol Psychiatry 33:415–422. https://doi.org/10.1016/0006-3223(93)90169-E
doi: 10.1016/0006-3223(93)90169-E
pubmed: 8490068
Kleiner M, Brainard D, Pelli D (2007) What’s new in Psychtoolbox-3? Perception 36. https://doi.org/10.1177/03010066070360S101
Kravitz DJ, Saleem KS, Baker CI et al (2013) The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn Sci 17:26–49. https://doi.org/10.1016/j.tics.2012.10.011
doi: 10.1016/j.tics.2012.10.011
pubmed: 23265839
Kravitz DJ, Saleem KS, Baker CI, Mishkin M (2011) A new neural framework for visuospatial processing. Nat Rev Neurosci 12:217–230. https://doi.org/10.1038/nrn3008
doi: 10.1038/nrn3008
pubmed: 21415848
pmcid: 3388718
Langner O, Dotsch R, Bijlstra G et al (2010) Presentation and validation of the Radboud Faces Database. Cogn Emot 24:1377–1388. https://doi.org/10.1080/02699930903485076
doi: 10.1080/02699930903485076
Leonova A, Pokorny J, Smith VC (2003) Spatial frequency processing in inferred PC- and MC-pathways. Vision Res 43:2133–2139. https://doi.org/10.1016/S0042-6989(03)00333-X
doi: 10.1016/S0042-6989(03)00333-X
pubmed: 12855249
Liebowitz MR (1987) Social Phobia. Mod Probl Pharmacopsychiatry 22:141–173. https://doi.org/10.1159/000414022
Livingstone M, Hubel D (1988) Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240:740–749. https://doi.org/10.1126/science.3283936
doi: 10.1126/science.3283936
pubmed: 3283936
Loftus GR, Harley EM (2004) How different spatial-frequency components contribute to visual information acquisition. J Exp Psychol Hum Percept Perform 30:104–118. https://doi.org/10.1037/0096-1523.30.1.104
doi: 10.1037/0096-1523.30.1.104
pubmed: 14769071
Mackey S, Allgaier N, Chaarani B et al (2019) Mega-analysis of gray matter volume in substance dependence: general and substance-specific regional effects. Am J Psychiatry 176:119–128. https://doi.org/10.1176/appi.ajp.2018.17040415
doi: 10.1176/appi.ajp.2018.17040415
pubmed: 30336705
Macmillan NA, Creelman CD (2004) Detection Theory: A User’s Guide, 2nd ed. Psychology Press, New York. https://doi.org/10.4324/9781410611147
Martino F, Castro-Torres JJ, Casares-López M et al (2021) Deterioration of binocular vision after alcohol intake influences driving performance. Sci Rep 11:8904. https://doi.org/10.1038/s41598-021-88435-w
doi: 10.1038/s41598-021-88435-w
pubmed: 33903669
pmcid: 8076280
Martins ICVDS, Souza GDS, Brasil A et al (2019) Psychophysical evaluation of visual functions of ex-alcoholic subjects after prolonged abstinence. Front Neurosci 13:179. https://doi.org/10.3389/fnins.2019.00179
doi: 10.3389/fnins.2019.00179
Mergler D, Blain L, Lemaire J, Lalande F (1988) Colour vision impairment and alcohol consumption. Neurotoxicol Teratol 10:255–260. https://doi.org/10.1016/0892-0362(88)90025-6
doi: 10.1016/0892-0362(88)90025-6
pubmed: 3211104
Merigan WH, Maunsell JH (1993) How parallel are the primate visual pathways? Annu Rev Neurosci 16:369–402. https://doi.org/10.1146/annurev.ne.16.030193.002101
doi: 10.1146/annurev.ne.16.030193.002101
pubmed: 8460898
Miller GA, Chapman JP (2001) Misunderstanding analysis of covariance. J Abnorm Psychol 110:40–48. https://doi.org/10.1037/0021-843X.110.1.40
doi: 10.1037/0021-843X.110.1.40
pubmed: 11261398
Morrison DJ, Schyns PG (2001) Usage of spatial scales for the categorization of faces, objects, and scenes. Psychon Bull Rev 8:454–469. https://doi.org/10.3758/BF03196180
doi: 10.3758/BF03196180
pubmed: 11700896
Newen A, Vetter P (2017) Why cognitive penetration of our perceptual experience is still the most plausible account. Conscious Cogn 47:26–37. https://doi.org/10.1016/j.concog.2016.09.005
doi: 10.1016/j.concog.2016.09.005
pubmed: 27667320
Nirody JA (2014) Development of spatial coarse-to-fine processing in the visual pathway. J Comput Neurosci 36:401–414. https://doi.org/10.1007/s10827-013-0480-6
doi: 10.1007/s10827-013-0480-6
pubmed: 24077933
Panichello MF, Cheung OS, Bar M (2013) Predictive feedback and conscious visual experience. Front Psychol 3:620. https://doi.org/10.3389/fpsyg.2012.00620
doi: 10.3389/fpsyg.2012.00620
pubmed: 23346068
pmcid: 3549576
Phelps EA, Ling S, Carrasco M (2006) Emotion facilitates perception and potentiates the perceptual benefits of attention. Psychol Sci 17:292–299. https://doi.org/10.1111/j.1467-9280.2006.01701.x
doi: 10.1111/j.1467-9280.2006.01701.x
pubmed: 16623685
Pillunat LE, Christ T, Luderer HJ, Stodtmeister R (1985) Flicker fusion frequency and organic syndrome in alcoholics. Percept Mot Skills 60:487–494. https://doi.org/10.2466/pms.1985.60.2.487
doi: 10.2466/pms.1985.60.2.487
pubmed: 4000866
Purushothaman G, Chen X, Yampolsky D, Casagrande VA (2014) Neural mechanisms of coarse-to-fine discrimination in the visual cortex. J Neurophysiol 112:2822–2833. https://doi.org/10.1152/jn.00612.2013
doi: 10.1152/jn.00612.2013
pubmed: 25210162
pmcid: 4254879
Rando K, Hong K-I, Bhagwagar Z et al (2011) Association of frontal and posterior cortical gray matter volume with time to alcohol relapse: a prospective study. Am J Psychiatry 168:183–192. https://doi.org/10.1176/appi.ajp.2010.10020233
doi: 10.1176/appi.ajp.2010.10020233
pubmed: 21078704
Roquelaure Y, Le Gargasson JF, Kupper S et al (1995) Alcohol consumption and visual contrast sensitivity. Alcohol Alcohol 30:681–685. https://doi.org/10.1093/oxfordjournals.alcalc.a045781
doi: 10.1093/oxfordjournals.alcalc.a045781
pubmed: 8554654
Spielberger CD, Gorsuch RL, Lusthene R et al (1983) Manual for the state-trait anxiety inventory. Consulting Psychology Press, Palo Alto
Vinogradov S, Fisher M, de Villers-Sidani E (2012) Cognitive training for impaired neural systems in neuropsychiatric illness. Neuropsychopharmacology 37:43–76. https://doi.org/10.1038/npp.2011.251
doi: 10.1038/npp.2011.251
pubmed: 22048465
Vuilleumier P, Armony JL, Driver J, Dolan RJ (2003) Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat Neurosci 6:624–631. https://doi.org/10.1038/nn1057
doi: 10.1038/nn1057
pubmed: 12740580
Wandell BA (1995) Foundations of vision. Sinauer Associates, Sunderland, Massachussetts
Wang J, Fan Y, Dong Y et al (2018) Combining gray matter volume in the cuneus and the cuneus-prefrontal connectivity may predict early relapse in abstinent alcohol-dependent patients. PLoS ONE 13:e0196860. https://doi.org/10.1371/journal.pone.0196860
doi: 10.1371/journal.pone.0196860
pubmed: 29734343
pmcid: 5937790
Wegner AJ, Gunthner A, Fahle M (2001) Visual performance and recovery in recently detoxified alcoholics. Alcohol Alcohol 36:171–179. https://doi.org/10.1093/alcalc/36.2.171
doi: 10.1093/alcalc/36.2.171
pubmed: 11259215
Willenbockel V, Sadr J, Fiset D et al (2010) Controlling low-level image properties: The SHINE toolbox. Behav Res Methods 42:671–684. https://doi.org/10.3758/BRM.42.3.671
doi: 10.3758/BRM.42.3.671
pubmed: 20805589
Williams DE (1984) Visual electrophysiology and psychophysics in chronic alcoholics and in patients on tuberculostatic chemotherapy. Am J Optom Physiol Opt 61:576–585. https://doi.org/10.1097/00006324-198409000-00007
doi: 10.1097/00006324-198409000-00007
pubmed: 6507577
Winston JS, Vuilleumier P, Dolan RJ (2003) Effects of low-spatial frequency components of fearful faces on fusiform cortex activity. Curr Biol 13:1824–1829. https://doi.org/10.1016/j.cub.2003.09.038
doi: 10.1016/j.cub.2003.09.038
pubmed: 14561410