Skip to main content Accessibility help
×
Home

Effects of multisensory integration processes on response inhibition in adolescent autism spectrum disorder

  • W. X. Chmielewski (a1), N. Wolff (a1), M. Mückschel (a1), V. Roessner (a1) and C. Beste (a1) (a2)...

Abstract

Background

In everyday life it is often required to integrate multisensory input to successfully conduct response inhibition (RI) and thus major executive control processes. Both RI and multisensory processes have been suggested to be altered in autism spectrum disorder (ASD). It is, however, unclear which neurophysiological processes relate to changes in RI in ASD and in how far these processes are affected by possible multisensory integration deficits in ASD.

Method

Combining high-density EEG recordings with source localization analyses, we examined a group of adolescent ASD patients (n = 20) and healthy controls (n = 20) using a novel RI task.

Results

Compared to controls, RI processes are generally compromised in adolescent ASD. This aggravation of RI processes is modulated by the content of multisensory information. The neurophysiological data suggest that deficits in ASD emerge in attentional selection and resource allocation processes related to occipito-parietal and middle frontal regions. Most importantly, conflict monitoring subprocesses during RI were specifically modulated by content of multisensory information in the superior frontal gyrus.

Conclusions

RI processes are overstrained in adolescent ASD, especially when conflicting multisensory information has to be integrated to perform RI. It seems that the content of multisensory input is important to consider in ASD and its effects on cognitive control processes.

Copyright

Corresponding author

*Address for correspondence: Dr C. Beste, Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine of the TU Dresden, Schubertstrasse 42, D-01309 Dresden, Germany. (Email: christian.beste@uniklinikum-dresden.de)

References

Hide All
APA (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th edn. American Psychiatric Publishing: Arlington, VA.
Aschenbach, TM (1991). Integrative Guide for the 1991CBCL/4-18, YSR, and TRF Profiles. Department of Psychiatry: University of Vermont.
Bari, A, Robbins, TW (2013). Inhibition and impulsivity: behavioral and neural basis of response control. Progress in Neurobiology 108, 4479.
Baum, SH, Stevenson, RA, Wallace, MT (2015). Behavioral, perceptual, and neural alterations in sensory and multisensory function in autism spectrum disorder. Progress in Neurobiology, 140160.
Bertone, A, Mottron, L, Jelenic, P, Faubert, J (2005). Enhanced and diminished visuo-spatial information processing in autism depends on stimulus complexity. Brain 128, 24302441.
Beste, C, Dziobek, I, Hielscher, H, Willemssen, R, Falkenstein, M (2009). Effects of stimulus-response compatibility on inhibitory processes in Parkinson's disease. European Journal of Neuroscience 29, 855860.
Beste, C, Ness, V, Falkenstein, M, Saft, C (2011). On the role of fronto-striatal neural synchronization processes for response inhibition–evidence from ERP phase-synchronization analyses in pre-manifest Huntington's disease gene mutation carriers. Neuropsychologia 49, 34843493.
Beste, C, Saft, C (2015). Action selection in a possible model of striatal medium spiny neuron dysfunction: behavioral and EEG data in a patient with benign hereditary chorea. Brain Structure and Function 220, 221228.
Beste, C, Willemssen, R, Saft, C, Falkenstein, M (2010). Response inhibition subprocesses and dopaminergic pathways: basal ganglia disease effects. Neuropsychologia 48, 366373.
Bishop, DVM, Norbury, CF (2005). Executive functions in children with communication impairments, in relation to autistic symptomatology 2: response inhibition. Autism 9, 2943.
Bokura, H, Yamaguchi, S, Kobayashi, S (2001). Electrophysiological correlates for response inhibition in a Go/NoGo task. Clinical Neurophysiology 112, 22242232.
Bruin, KJ, Wijers, AA, van Staveren, AS (2001). Response priming in a go/nogo task: do we have to explain the go/nogo N2 effect in terms of response activation instead of inhibition? Clinical Neurophysiology 112, 16601671.
Campbell, J, Sharma, A (2013). Compensatory changes in cortical resource allocation in adults with hearing loss. Frontiers in Systems Neuroscience 7, 71.
Chmielewski, WX, Beste, C (2015). Action control processes in autism spectrum disorder – insights from a neurobiological and neuroanatomical perspective. Progress in Neurobiology 124, 4983.
Chmielewski, WX, Mückschel, M, Dippel, G, Beste, C (2015 a). Concurrent information affects response inhibition processes via the modulation of theta oscillations in cognitive control networks. Brain Structure and Function. doi:10.1007/s00429-015-1137-1.
Chmielewski, WX, Mückschel, M, Roessner, V, Beste, C (2014). Expectancy effects during response selection modulate attentional selection and inhibitory control networks. Behavioural Brain Research 274C, 5361.
Chmielewski, WX, Mückschel, M, Stock, A-K, Beste, C (2015 b). The impact of mental workload on inhibitory control subprocesses. NeuroImage 112, 96104.
Chmielewski, WX, Roessner, V, Beste, C (2015 c). Predictability and context determine differences in conflict monitoring between adolescence and adulthood. Behavioural Brain Research 292, 1018.
Cohen, MX (2014). Analyzing Neural Time Series Data. Theory and Practice. MIT Press.
Dilling, H, Mombour, W, Schmidt, MH, Schulte-Markwort, E, Remschmidt, H (eds) (2015). Internationale Klassifikation psychischer Störungen ICD-10 Kapitel V (F). Klinisch-diagnostische Leitlinien. Huber: Bern.
Dippel, G, Beste, C (2015). A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour. Nature Communications 6, 6587.
Duerden, EG, Taylor, MJ, Soorya, LV, Wang, T, Fan, J, Anagnostou, E (2013). Neural correlates of inhibition of socially relevant stimuli in adults with autism spectrum disorder. Brain Research 1533, 8090.
Falkenstein, M, Hoormann, J, Hohnsbein, J (1999). ERP components in Go/Nogo tasks and their relation to inhibition. Acta Psychologica 101, 267291.
Foxe, JJ, Molholm, S, Del Bene, VA, Frey, H-P, Russo, NN, Blanco, D, Saint-Amour, D, Ross, LA (2015). Severe multisensory speech integration deficits in high-functioning school-aged children with Autism Spectrum Disorder (ASD) and their resolution during early adolescence. Cerebral Cortex (New York) 25, 298312.
Friedman, D, Cycowicz, YM, Gaeta, H (2001). The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty. Neuroscience and Biobehavioral Reviews 25, 355373.
Fuchs, M, Kastner, J, Wagner, M, Hawes, S, Ebersole, JS (2002). A standardized boundary element method volume conductor model. Clinical Neurophysiology 113, 702712.
Geisler, MW, Murphy, C (2000). Event-related brain potentials to attended and ignored olfactory and trigeminal stimuli. International Journal of Psychophysiology 37, 309315.
Geurts, HM, Verté, S, Oosterlaan, J, Roeyers, H, Sergeant, JA (2004). How specific are executive functioning deficits in attention deficit hyperactivity disorder and autism? Journal of Child Psychology and Psychiatry 45, 836854.
Gotham, K, Pickles, A, Lord, C (2009). Standardizing ADOS scores for a measure of severity in autism spectrum disorders. Journal of Autism and Developmental Disorders 39, 693705.
Gotham, K, Risi, S, Pickles, A, Lord, C (2007). The autism diagnostic observation schedule: revised algorithms for improved diagnostic validity. Journal of Autism and Developmental Disorders 37, 613627.
Herrmann, CS, Knight, RT (2001). Mechanisms of human attention: event-related potentials and oscillations. Neuroscience and Biobehavioral Reviews 25, 465476.
Hughes, C (1996). Control of action and thought: normal development and dysfunction in autism: a research note. Journal of Child Psychology and Psychiatry 37, 229236.
Huster, RJ, Enriquez-Geppert, S, Lavallee, CF, Falkenstein, M, Herrmann, CS (2013). Electroencephalography of response inhibition tasks: functional networks and cognitive contributions. International Journal of Psychophysiology 87, 217233.
Jodo, E, Kayama, Y (1992). Relation of a negative ERP component to response inhibition in a Go/No-go task. Electroencephalography and Clinical Neurophysiology 82, 477482.
Kana, RK, Keller, TA, Minshew, NJ, Just, MA (2007). Inhibitory control in high-functioning autism: decreased activation and underconnectivity in inhibition networks. Biological Psychiatry 62, 198206.
Kok, A (1986). Effects of degradation of visual stimuli on components of the event-related potential (ERP) in go/nogo reaction tasks. Biological Psychology 23, 2138.
Kwakye, LD, Foss-Feig, JH, Cascio, CJ, Stone, WL, Wallace, MT (2011). Altered auditory and multisensory temporal processing in autism spectrum disorders. Frontiers in Integrative Neuroscience 4, 129.
Lee, PS, Yerys, BE, Rosa, AD, Foss-Feig, J, Barnes, KA, James, JD, VanMeter, J, Vaidya, CJ, Gaillard, WD, Kenworthy, LE (2009). Functional connectivity of the inferior frontal cortex changes with age in children with autism spectrum disorders: a fcMRI study of response inhibition. Cerebral Cortex 19, 17871794.
Lord, C, Risi, S (1998). Frameworks and methods in diagnosing autism spectrum disorders. Mental Retardation and Developmental Disabilities Research Reviews 4, 9096.
Lord, C, Rutter, M, Couteur, AL (1994). Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders 24, 659685.
Makeig, S, Bell, AJ, Jung, T-P, Sejnowski, TJ (1996). Independent component analysis of electroencephalographic data. In Advances in Neural Information Processing Systemss, Vol. 8 (ed. Touretzky, D.S.), pp. 141151. MIT Press: Cambridge, Massachsetts, USA.
Mazziotta, J, Toga, A, Evans, A, Fox, P, Lancaster, J, Zilles, K, Woods, R, Paus, T, Simpson, G, Pike, B, Holmes, C, Collins, L, Thompson, P, MacDonald, D, Iacoboni, M, Schormann, T, Amunts, K, Palomero-Gallagher, N, Geyer, S, Parsons, L, Narr, K, Kabani, N, Le Goualher, G, Boomsma, D, Cannon, T, Kawashima, R, Mazoyer, B (2001). A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philosophical Transactions of the Royal Society of London. Series B 356, 12931322.
Menon, V, Adleman, NE, White, CD, Glover, GH, Reiss, AL (2001). Error-related brain activation during a Go/NoGo response inhibition task. Human Brain Mapping 12, 131143.
Minshew, NJ, Hobson, JA (2008). Sensory sensitivities and performance on sensory perceptual tasks in high-functioning individuals with autism. Journal of Autism and Developmental Disorders 38, 14851498.
Mückschel, M, Smitka, M, Hermann, A, von der Hagen, M, Beste, C (2015). Deep brain stimulation in the globus pallidus compensates response inhibition deficits: evidence from pantothenate kinase-associated neurodegeneration. Brain Structure and Function 221, 22512257.
Mückschel, M, Stock, A-K, Beste, C (2014). Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cerebral Cortex 24, 21202129.
Nieuwenhuis, S, Yeung, N, Cohen, JD (2004). Stimulus modality, perceptual overlap, and the go/no-go N2. Psychophysiology 41, 157160.
Nieuwenhuis, S, Yeung, N, van den Wildenberg, W, Ridderinkhof, KR (2003). Electrophysiological correlates of anterior cingulate function in a go/no-go task: effects of response conflict and trial type frequency. Cognitive, Affective, and Behavioral Neuroscience 3, 1726.
Nunez, PL, Pilgreen, KL (1991). The spline-Laplacian in clinical neurophysiology: a method to improve EEG spatial resolution. Journal of Clinical Neurophysiology 8, 397413.
Ozonoff, S, Strayer, DL, McMahon, WM, Filloux, F (1994). Executive function abilities in autism and tourette syndrome: an information processing approach. Journal of Child Psychology and Psychiatry 35, 10151032.
Pascual-Marqui, RD (2002). Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods and Findings in Experimental and Clinical Pharmacology 24(Suppl. D), 512.
Peelle, JE, Troiani, V, Wingfield, A, Grossman, M (2010). Neural processing during older adults’ comprehension of spoken sentences: age differences in resource allocation and connectivity. Cerebral Cortex (New York, N.Y.: 1991) 20, 773782.
Petermann, F, Petermann, U (2011). Wechsler Intelligence Scale for Children, 4th edn. Pearson Assessment: Frankfurt/Main.
Pfefferbaum, A, Ford, JM, Weller, BJ, Kopell, BS (1985). ERPs to response production and inhibition. Electroencephalography and Clinical Neurophysiology 60, 423434.
Quetscher, C, Yildiz, A, Dharmadhikari, S, Glaubitz, B, Schmidt-Wilcke, T, Dydak, U, Beste, C (2015). Striatal GABA-MRS predicts response inhibition performance and its cortical electrophysiological correlates. Brain Structure and Function 220, 35553564.
Raymaekers, R, van der Meere, J, Roeyers, H (2004). Event-rate manipulation and its effect on arousal modulation and response inhibition in adults with high functioning autism. Journal of Clinical and Experimental Neuropsychology 26, 7482.
Roche, RAP, Garavan, H, Foxe, JJ, O'Mara, SM (2004). Individual differences discriminate event-related potentials but not performance during response inhibition. Experimental Brain Research 160, 6070.
Salazar, RF, Kayser, C, König, P (2004). Effects of training on neuronal activity and interactions in primary and higher visual cortices in the alert cat. Journal of Neuroscience 24, 16271636.
Schintu, S, Hadj-Bouziane, F, Dal Monte, O, Knutson, KM, Pardini, M, Wassermann, EM, Grafman, J, Krueger, F (2014). Object and space perception – is it a matter of hemisphere? Cortex 57, 244253.
Schmajuk, M, Liotti, M, Busse, L, Woldorff, MG (2006). Electrophysiological activity underlying inhibitory control processes in normal adults. Neuropsychologia 44, 384395.
Schmitz, N, Rubia, K, Daly, E, Smith, A, Williams, S, Murphy, DGM (2006). Neural correlates of executive function in autistic spectrum disorders. Biological Psychiatry 59, 716.
Sekihara, K, Sahani, M, Nagarajan, SS (2005). Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction. NeuroImage 25, 10561067.
Sheehan, DV, Sheehan, KH, Shytle, RD, Janavs, J, Bannon, Y, Rogers, JE, Milo, KM, Stock, SL, Wilkinson, B (2010). Reliability and validity of the mini international neuropsychiatric interview for children and adolescents (MINI-KID). Journal of Clinical Psychiatry 71, 313326.
Shumway, S, Farmer, C, Thurm, A, Joseph, L, Black, D, Golden, C (2012). The ADOS calibrated severity score: relationship to phenotypic variables and stability over time. Autism Research 5, 267276.
Simson, R, Vaughan, HG Jr., Ritter, W (1977). The scalp topography of potentials in auditory and visual discrimination tasks. Electroencephalography and Clinical Neurophysiology 42, 528535.
Stevenson, RA, Siemann, JK, Woynaroski, TG, Schneider, BC, Eberly, HE, Camarata, SM, Wallace, MT (2014). Evidence for diminished multisensory integration in autism spectrum disorders. Journal of Autism and Developmental Disorders 44, 31613167.
Sugimoto, F, Katayama, J (2013). Somatosensory P2 reflects resource allocation in a game task: assessment with an irrelevant probe technique using electrical probe stimuli to shoulders. International Journal of Psychophysiology 87, 200204.
Wessel, JR, Aron, AR (2015). It's not too late: the onset of the frontocentral P3 indexes successful response inhibition in the stop-signal paradigm. Psychophysiology 52, 472480.

Keywords

Type Description Title
WORD
Supplementary materials

Chmielewski supplementary material
Figures S1-S2

 Word (2.0 MB)
2.0 MB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed