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Published in: Journal of Neurodevelopmental Disorders 1/2024

Open Access 01-12-2024 | Autism Spectrum Disorder | Research

Neurofeedback training of executive function in autism spectrum disorder: distinct effects on brain activity levels and compensatory connectivity changes

Authors: Daniela Jardim Pereira, Sofia Morais, Alexandre Sayal, João Pereira, Sofia Meneses, Graça Areias, Bruno Direito, António Macedo, Miguel Castelo-Branco

Published in: Journal of Neurodevelopmental Disorders | Issue 1/2024

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Abstract

Background

Deficits in executive function (EF) are consistently reported in autism spectrum disorders (ASD). Tailored cognitive training tools, such as neurofeedback, focused on executive function enhancement might have a significant impact on the daily life functioning of individuals with ASD. We report the first real-time fMRI neurofeedback (rt-fMRI NF) study targeting the left dorsolateral prefrontal cortex (DLPFC) in ASD.

Methods

Thirteen individuals with autism without intellectual disability and seventeen neurotypical individuals completed a rt-fMRI working memory NF paradigm, consisting of subvocal backward recitation of self-generated numeric sequences. We performed a region-of-interest analysis of the DLPFC, whole-brain comparisons between groups and, DLPFC-based functional connectivity.

Results

The ASD and control groups were able to modulate DLPFC activity in 84% and 98% of the runs. Activity in the target region was persistently lower in the ASD group, particularly in runs without neurofeedback. Moreover, the ASD group showed lower activity in premotor/motor areas during pre-neurofeedback run than controls, but not in transfer runs, where it was seemingly balanced by higher connectivity between the DLPFC and the motor cortex. Group comparison in the transfer run also showed significant differences in DLPFC-based connectivity between groups, including higher connectivity with areas integrated into the multidemand network (MDN) and the visual cortex.

Conclusions

Neurofeedback seems to induce a higher between-group similarity of the whole-brain activity levels (including the target ROI) which might be promoted by changes in connectivity between the DLPFC and both high and low-level areas, including motor, visual and MDN regions.
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Literature
1.
go back to reference Hill EL. Evaluating the theory of executive dysfunction in autism. Develop Rev. 2004;24(2):189–233.CrossRef Hill EL. Evaluating the theory of executive dysfunction in autism. Develop Rev. 2004;24(2):189–233.CrossRef
2.
go back to reference Demetriou EA, Lampit A, Quintana DS, Naismith SL, Song YJC, Pye JE, et al. Autism spectrum disorders: A meta-analysis of executive function. Mol Psychiatry. 2018;23(5):1198–204.PubMedCrossRef Demetriou EA, Lampit A, Quintana DS, Naismith SL, Song YJC, Pye JE, et al. Autism spectrum disorders: A meta-analysis of executive function. Mol Psychiatry. 2018;23(5):1198–204.PubMedCrossRef
4.
go back to reference Habib A, Harris L, Pollick F, Melville C. A meta-analysis of working memory in individuals with autism spectrum disorders. PLoS One. 2019;14(4) Habib A, Harris L, Pollick F, Melville C. A meta-analysis of working memory in individuals with autism spectrum disorders. PLoS One. 2019;14(4)
5.
go back to reference Enriquez-Geppert S, Huster RJ, Herrmann CS. Boosting brain functions: Improving executive functions with behavioral training, neurostimulation, and neurofeedback. Int J Psychophysiol. 2013;88(1):1–16.PubMedCrossRef Enriquez-Geppert S, Huster RJ, Herrmann CS. Boosting brain functions: Improving executive functions with behavioral training, neurostimulation, and neurofeedback. Int J Psychophysiol. 2013;88(1):1–16.PubMedCrossRef
6.
go back to reference Russell J. Autism as an executive disorder. Oxford University Press; 1997. Russell J. Autism as an executive disorder. Oxford University Press; 1997.
10.
go back to reference Ahuja A, Rodriguez NY. Is the Dorsolateral Prefrontal Cortex Actually Several Different Brain Areas? J Neurosci Soc Neurosci. 2022;42:6310–2. Ahuja A, Rodriguez NY. Is the Dorsolateral Prefrontal Cortex Actually Several Different Brain Areas? J Neurosci Soc Neurosci. 2022;42:6310–2.
11.
go back to reference Rabinovici GD, Stephens ML, Possin KL. Executive dysfunction. Contin Lifelong Learning in Neurol. 2015;21(3):646–59.CrossRef Rabinovici GD, Stephens ML, Possin KL. Executive dysfunction. Contin Lifelong Learning in Neurol. 2015;21(3):646–59.CrossRef
12.
go back to reference Guan M, Ma L, Li L, Yan B, Zhao L, Tong L, et al. Self-regulation of brain activity in patients with postherpetic neuralgia: A double-blind randomized study using real-time fMRI neurofeedback. PLoS One. 2015;10(4):1–14.CrossRef Guan M, Ma L, Li L, Yan B, Zhao L, Tong L, et al. Self-regulation of brain activity in patients with postherpetic neuralgia: A double-blind randomized study using real-time fMRI neurofeedback. PLoS One. 2015;10(4):1–14.CrossRef
13.
go back to reference Jung JY, Lambon Ralph MA, Jackson RL. Subregions of DLPFC Display Graded yet Distinct Structural and Functional Connectivity. J Neurosci. 2022;42(15):3241–52.PubMedPubMedCentralCrossRef Jung JY, Lambon Ralph MA, Jackson RL. Subregions of DLPFC Display Graded yet Distinct Structural and Functional Connectivity. J Neurosci. 2022;42(15):3241–52.PubMedPubMedCentralCrossRef
15.
go back to reference Camilleri JA, Müller VI, Fox P, Laird AR, Hoffstaedter F, Kalenscher T, et al. Definition and characterization of an extended multiple-demand network. Neuroimage. 2018;15(165):138–47.CrossRef Camilleri JA, Müller VI, Fox P, Laird AR, Hoffstaedter F, Kalenscher T, et al. Definition and characterization of an extended multiple-demand network. Neuroimage. 2018;15(165):138–47.CrossRef
16.
go back to reference Zhang Z, Peng P, Zhang D. Executive Function in High-Functioning Autism Spectrum Disorder: A Meta-analysis of fMRI Studies. J Autism Dev Disord. 2020;50(11):4022–38.PubMedCrossRef Zhang Z, Peng P, Zhang D. Executive Function in High-Functioning Autism Spectrum Disorder: A Meta-analysis of fMRI Studies. J Autism Dev Disord. 2020;50(11):4022–38.PubMedCrossRef
17.
go back to reference Maximo JO, Kana RK. Aberrant “deep connectivity” in autism: A cortico–subcortical functional connectivity magnetic resonance imaging study. Autism Res. 2019;12(3):384–400.PubMedCrossRef Maximo JO, Kana RK. Aberrant “deep connectivity” in autism: A cortico–subcortical functional connectivity magnetic resonance imaging study. Autism Res. 2019;12(3):384–400.PubMedCrossRef
18.
go back to reference Koshino H, Carpenter PA, Minshew NJ, Cherkassky VL, Keller TA, Just MA. Functional connectivity in an fMRI working memory task in high-functioning autism. Neuroimage. 2005;24(3):810–21. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1053811904005567PubMedCrossRef Koshino H, Carpenter PA, Minshew NJ, Cherkassky VL, Keller TA, Just MA. Functional connectivity in an fMRI working memory task in high-functioning autism. Neuroimage. 2005;24(3):810–21. Available from: https://​linkinghub.​elsevier.​com/​retrieve/​pii/​S105381190400556​7PubMedCrossRef
21.
go back to reference Direito B, Mouga S, Sayal A, Simões M, Quental H, Bernardino I, et al. Training the social brain: Clinical and neural effects of an 8-week real-time functional magnetic resonance imaging neurofeedback Phase IIa Clinical Trial in Autism. Autism. 2021;25(6):1746–60.PubMedCrossRef Direito B, Mouga S, Sayal A, Simões M, Quental H, Bernardino I, et al. Training the social brain: Clinical and neural effects of an 8-week real-time functional magnetic resonance imaging neurofeedback Phase IIa Clinical Trial in Autism. Autism. 2021;25(6):1746–60.PubMedCrossRef
22.
go back to reference Pereira JA, Sepulveda P, Rana M, Montalba C, Tejos C, Torres R, et al. Self-Regulation of the Fusiform Face Area in Autism Spectrum: A Feasibility Study With Real-Time fMRI Neurofeedback. Front Hum Neurosci. 2019;20:13. Pereira JA, Sepulveda P, Rana M, Montalba C, Tejos C, Torres R, et al. Self-Regulation of the Fusiform Face Area in Autism Spectrum: A Feasibility Study With Real-Time fMRI Neurofeedback. Front Hum Neurosci. 2019;20:13.
23.
go back to reference Mouga S, Duarte IC, Café C, Sousa D, Duque F, Oliveira G, et al. Attentional Cueing and Executive Deficits Revealed by a Virtual Supermarket Task Coupled With Eye-Tracking in Autism Spectrum Disorder. Front Psychol. 2021;31:12. Mouga S, Duarte IC, Café C, Sousa D, Duque F, Oliveira G, et al. Attentional Cueing and Executive Deficits Revealed by a Virtual Supermarket Task Coupled With Eye-Tracking in Autism Spectrum Disorder. Front Psychol. 2021;31:12.
24.
go back to reference Boyd BA, McBee M, Holtzclaw T, Baranek GT, Bodfish JW. Relationships among repetitive behaviors, sensory features, and executive functions in high functioning autism. Res Autism Spectr Disord. 2009;3(4):959–66.PubMedPubMedCentralCrossRef Boyd BA, McBee M, Holtzclaw T, Baranek GT, Bodfish JW. Relationships among repetitive behaviors, sensory features, and executive functions in high functioning autism. Res Autism Spectr Disord. 2009;3(4):959–66.PubMedPubMedCentralCrossRef
28.
go back to reference Zhang G, Yao L, Zhao X. Neural effect of real time fMRI based working memory neurofeedback training on the cortico-subcortico-cerebellar circuit. J Med Imaging Health Inform. 2016;6(5):1324–9.CrossRef Zhang G, Yao L, Zhao X. Neural effect of real time fMRI based working memory neurofeedback training on the cortico-subcortico-cerebellar circuit. J Med Imaging Health Inform. 2016;6(5):1324–9.CrossRef
29.
go back to reference Weiss F, Zhang J, Aslan A, Kirsch P, Gerchen MF. Feasibility of training the dorsolateral prefrontal-striatal network by real-time fMRI neurofeedback. Sci Rep. 2022;12(1) Weiss F, Zhang J, Aslan A, Kirsch P, Gerchen MF. Feasibility of training the dorsolateral prefrontal-striatal network by real-time fMRI neurofeedback. Sci Rep. 2022;12(1)
30.
go back to reference Weiss F, Zamoscik V, Schmidt SNL, Halli P, Kirsch P, Gerchen MF. Just a very expensive breathing training? Risk of respiratory artefacts in functional connectivity-based real-time fMRI neurofeedback. Neuroimage. 2020;15:210. Weiss F, Zamoscik V, Schmidt SNL, Halli P, Kirsch P, Gerchen MF. Just a very expensive breathing training? Risk of respiratory artefacts in functional connectivity-based real-time fMRI neurofeedback. Neuroimage. 2020;15:210.
31.
go back to reference Weschler D. Weschler Adult Intelligence Scale (WAIS-III) - Portuguese version (Ferreira C, Machado A, Rocha AM). Lisboa: CECOG; 2008. Weschler D. Weschler Adult Intelligence Scale (WAIS-III) - Portuguese version (Ferreira C, Machado A, Rocha AM). Lisboa: CECOG; 2008.
32.
go back to reference American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th ed. Washington D.C.; 2013. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th ed. Washington D.C.; 2013.
33.
go back to reference Lord C, Rutter M, DiLavore PC, Risi S, Gotham K, Bishop S. Autism Diagnostic Observation Schedule, second edition (ADOS-2). Torrance, CA: Western Psychological Services; 2012. Lord C, Rutter M, DiLavore PC, Risi S, Gotham K, Bishop S. Autism Diagnostic Observation Schedule, second edition (ADOS-2). Torrance, CA: Western Psychological Services; 2012.
35.
go back to reference Ros T, Enriquez-Geppert S, Zotev V, Young KD, Wood G, Whitfield-Gabrieli S, et al. Consensus on the reporting and experimental design of clinical and cognitive-behavioural neurofeedback studies (CRED-nf checklist). Brain. 2020;143(6):1674–85.PubMedPubMedCentralCrossRef Ros T, Enriquez-Geppert S, Zotev V, Young KD, Wood G, Whitfield-Gabrieli S, et al. Consensus on the reporting and experimental design of clinical and cognitive-behavioural neurofeedback studies (CRED-nf checklist). Brain. 2020;143(6):1674–85.PubMedPubMedCentralCrossRef
36.
go back to reference Emch M, von Bastian CC, Koch K. Neural correlates of verbal working memory: An fMRI meta-analysis. Front Hum Neurosci. 2019;13:1–17.CrossRef Emch M, von Bastian CC, Koch K. Neural correlates of verbal working memory: An fMRI meta-analysis. Front Hum Neurosci. 2019;13:1–17.CrossRef
39.
go back to reference Nieto-Castanon A. Handbook of functional connectivity Magnetic Resonance Imaging methods in CONN. In: Handbook of functional connectivity Magnetic Resonance Imaging methods in CONN. Hilbert Press; 2020.CrossRef Nieto-Castanon A. Handbook of functional connectivity Magnetic Resonance Imaging methods in CONN. In: Handbook of functional connectivity Magnetic Resonance Imaging methods in CONN. Hilbert Press; 2020.CrossRef
40.
go back to reference Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp. 1996;4(1):58–73.PubMedCrossRef Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp. 1996;4(1):58–73.PubMedCrossRef
41.
go back to reference Philip RCM, Dauvermann MR, Whalley HC, Baynham K, Lawrie SM, Stanfield AC. A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neurosci Biobehav Rev. 2012;36:901–42. Philip RCM, Dauvermann MR, Whalley HC, Baynham K, Lawrie SM, Stanfield AC. A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neurosci Biobehav Rev. 2012;36:901–42.
42.
go back to reference Beauregard M, Lévesque J. Functional magnetic resonance imaging investigation of the effects of neurofeedback training on the neural bases of selective attention and response inhibition in children with attention-deficit/hyperactivity disorder. Appl Psychophysiol Biofeedback. 2006;31(1):3–20.PubMedCrossRef Beauregard M, Lévesque J. Functional magnetic resonance imaging investigation of the effects of neurofeedback training on the neural bases of selective attention and response inhibition in children with attention-deficit/hyperactivity disorder. Appl Psychophysiol Biofeedback. 2006;31(1):3–20.PubMedCrossRef
43.
go back to reference Sitaram R, Veit R, Stevens B, Caria A, Gerloff C, Birbaumer N, et al. Acquired control of ventral premotor cortex activity by feedback training: An exploratory real-time fMRI and TMS study. Neurorehabil Neural Repair. 2012;26(3):256–65.PubMedCrossRef Sitaram R, Veit R, Stevens B, Caria A, Gerloff C, Birbaumer N, et al. Acquired control of ventral premotor cortex activity by feedback training: An exploratory real-time fMRI and TMS study. Neurorehabil Neural Repair. 2012;26(3):256–65.PubMedCrossRef
45.
go back to reference Haller S, Birbaumer N, Veit R. Real-time fMRI feedback training may improve chronic tinnitus. Eur Radiol. 2010;20(3):696–703.PubMedCrossRef Haller S, Birbaumer N, Veit R. Real-time fMRI feedback training may improve chronic tinnitus. Eur Radiol. 2010;20(3):696–703.PubMedCrossRef
48.
go back to reference Miotto EC, Savage CR, Evans JJ, Wilson BA, Martins MGM, Iaki S, et al. Bilateral activation of the prefrontal cortex after strategic semantic cognitive training. Hum Brain Mapp. 2006;27(4):288–95.PubMedCrossRef Miotto EC, Savage CR, Evans JJ, Wilson BA, Martins MGM, Iaki S, et al. Bilateral activation of the prefrontal cortex after strategic semantic cognitive training. Hum Brain Mapp. 2006;27(4):288–95.PubMedCrossRef
49.
go back to reference Brehmer Y, Rieckmann A, Bellander M, Westerberg H, Fischer H, Bäckman L. Neural correlates of training-related working-memory gains in old age. Neuroimage. 2011;58(4):1110–20.PubMedCrossRef Brehmer Y, Rieckmann A, Bellander M, Westerberg H, Fischer H, Bäckman L. Neural correlates of training-related working-memory gains in old age. Neuroimage. 2011;58(4):1110–20.PubMedCrossRef
53.
go back to reference Rajendran G, Mitchell P. Cognitive theories of autism. Developmental Review. 2007;27(2):224–60.CrossRef Rajendran G, Mitchell P. Cognitive theories of autism. Developmental Review. 2007;27(2):224–60.CrossRef
54.
go back to reference Umesawa Y, Atsumi T, Chakrabarty M, Fukatsu R, Ide M. GABA Concentration in the Left Ventral Premotor Cortex Associates With Sensory Hyper-Responsiveness in Autism Spectrum Disorders Without Intellectual Disability. Front Neurosci. 2020;19:14. Umesawa Y, Atsumi T, Chakrabarty M, Fukatsu R, Ide M. GABA Concentration in the Left Ventral Premotor Cortex Associates With Sensory Hyper-Responsiveness in Autism Spectrum Disorders Without Intellectual Disability. Front Neurosci. 2020;19:14.
55.
go back to reference Hau J, Kohli J S, Shryock I, Kinnear MK, Schadler A, Müller RA, et al. Supplementary and Premotor Aspects of the Corticospinal Tract Show Links with Restricted and Repetitive Behaviors in Middle-Aged Adults with Autism Spectrum Disorder. Cerebral Cortex. 2021;31(8):3962–72.PubMedPubMedCentral Hau J, Kohli J S, Shryock I, Kinnear MK, Schadler A, Müller RA, et al. Supplementary and Premotor Aspects of the Corticospinal Tract Show Links with Restricted and Repetitive Behaviors in Middle-Aged Adults with Autism Spectrum Disorder. Cerebral Cortex. 2021;31(8):3962–72.PubMedPubMedCentral
56.
go back to reference Ren J, Huang F, Zhou Y, Zhuang L, Xu J, Gao C, et al. The function of the hippocampus and middle temporal gyrus in forming new associations and concepts during the processing of novelty and usefulness features in creative designs. Neuroimage. 2020;1:214. Ren J, Huang F, Zhou Y, Zhuang L, Xu J, Gao C, et al. The function of the hippocampus and middle temporal gyrus in forming new associations and concepts during the processing of novelty and usefulness features in creative designs. Neuroimage. 2020;1:214.
57.
go back to reference Davey J, Thompson HE, Hallam G, Karapanagiotidis T, Murphy C, de Caso I, et al. Exploring the role of the posterior middle temporal gyrus in semantic cognition: Integration of anterior temporal lobe with executive processes. Neuroimage. 2016;15(137):165–77.CrossRef Davey J, Thompson HE, Hallam G, Karapanagiotidis T, Murphy C, de Caso I, et al. Exploring the role of the posterior middle temporal gyrus in semantic cognition: Integration of anterior temporal lobe with executive processes. Neuroimage. 2016;15(137):165–77.CrossRef
59.
go back to reference May KE, Kana RK. Frontoparietal Network in Executive Functioning in Autism Spectrum Disorder. Autism Res. 2020;13(10):1762–77.PubMedCrossRef May KE, Kana RK. Frontoparietal Network in Executive Functioning in Autism Spectrum Disorder. Autism Res. 2020;13(10):1762–77.PubMedCrossRef
60.
go back to reference Lombardo M v., Chakrabarti B, Bullmore ET, Sadek SA, Pasco G, Wheelwright SJ, et al. Atypical neural self-representation in autism. Brain. 2010;133(2):611–24. Lombardo M v., Chakrabarti B, Bullmore ET, Sadek SA, Pasco G, Wheelwright SJ, et al. Atypical neural self-representation in autism. Brain. 2010;133(2):611–24.
61.
go back to reference Wicker B, Fonlupt P, Hubert B, Tardif C, Gepner B, Deruelle C. Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neurosci. 2008;3(2):135–43.PubMedPubMedCentralCrossRef Wicker B, Fonlupt P, Hubert B, Tardif C, Gepner B, Deruelle C. Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neurosci. 2008;3(2):135–43.PubMedPubMedCentralCrossRef
62.
go back to reference Frith U. Autism: Explaining the enigma, 2nd ed. Malden: Blackwell Publishing; 2003. Frith U. Autism: Explaining the enigma, 2nd ed. Malden: Blackwell Publishing; 2003.
63.
go back to reference Villalobos ME, Mizuno A, Dahl BC, Kemmotsu N, Müller RA. Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism. Neuroimage. 2005;25(3):916–25.PubMedCrossRef Villalobos ME, Mizuno A, Dahl BC, Kemmotsu N, Müller RA. Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism. Neuroimage. 2005;25(3):916–25.PubMedCrossRef
64.
go back to reference Buckner RL, Andrews-Hanna JR, Schacter DL. The brain’s default network: Anatomy, function, and relevance to disease. Ann N Y Acad Sci. 2008;1124:1–38.PubMedCrossRef Buckner RL, Andrews-Hanna JR, Schacter DL. The brain’s default network: Anatomy, function, and relevance to disease. Ann N Y Acad Sci. 2008;1124:1–38.PubMedCrossRef
68.
go back to reference Kolk SM, Rakic P. Development of prefrontal cortex, vol. 47. Neuropsychopharmacology Springer Nature; 2022. p. 41–57. Kolk SM, Rakic P. Development of prefrontal cortex, vol. 47. Neuropsychopharmacology Springer Nature; 2022. p. 41–57.
69.
go back to reference Gogtay N, Giedd J, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proceed Nat Academ Sci. 2004;101(21):8174–9.CrossRef Gogtay N, Giedd J, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proceed Nat Academ Sci. 2004;101(21):8174–9.CrossRef
70.
go back to reference Tüdös Z, Hok P, Hluštík P, Grambal A. Functional MRI study of gender effects in brain activations during verbal working memory task. Physiol Res. 2018;67(5):825–9.PubMedCrossRef Tüdös Z, Hok P, Hluštík P, Grambal A. Functional MRI study of gender effects in brain activations during verbal working memory task. Physiol Res. 2018;67(5):825–9.PubMedCrossRef
71.
go back to reference Schmidt H, Jogia J, Fast K, Christodoulou T, Haldane M, Kumari V, et al. No gender differences in brain activation during the N-back task: An fMRI study in healthy individuals. Hum Brain Mapp. 2009;30(11):3609–15.PubMedPubMedCentralCrossRef Schmidt H, Jogia J, Fast K, Christodoulou T, Haldane M, Kumari V, et al. No gender differences in brain activation during the N-back task: An fMRI study in healthy individuals. Hum Brain Mapp. 2009;30(11):3609–15.PubMedPubMedCentralCrossRef
72.
go back to reference Supekar K, De Los AC, Ryali S, Cao K, Ma T, Menon V. Deep learning identifies robust gender differences in functional brain organization and their dissociable links to clinical symptoms in autism. British J Psychiat. 2022;220(4):202–9.CrossRef Supekar K, De Los AC, Ryali S, Cao K, Ma T, Menon V. Deep learning identifies robust gender differences in functional brain organization and their dissociable links to clinical symptoms in autism. British J Psychiat. 2022;220(4):202–9.CrossRef
73.
go back to reference Santos S, Ferreira H, Martins J, Gonçalves J, Castelo-Branco M. Male sex bias in early and late onset neurodevelopmental disorders: Shared aspects and differences in Autism Spectrum Disorder, Attention Deficit/hyperactivity Disorder, and Schizophrenia, vol. 135. Elsevier Ltd: Neuroscience and Biobehavioral Reviews; 2022. Santos S, Ferreira H, Martins J, Gonçalves J, Castelo-Branco M. Male sex bias in early and late onset neurodevelopmental disorders: Shared aspects and differences in Autism Spectrum Disorder, Attention Deficit/hyperactivity Disorder, and Schizophrenia, vol. 135. Elsevier Ltd: Neuroscience and Biobehavioral Reviews; 2022.
74.
go back to reference Loomes R, Hull L, Mandy WPL. What Is the Male-to-Female Ratio in Autism Spectrum Disorder? A Systematic Review and Meta-Analysis. In: Journal of the American Academy of Child and Adolescent Psychiatry, vol. 56. Elsevier Inc.; 2017. p. 466–74. Loomes R, Hull L, Mandy WPL. What Is the Male-to-Female Ratio in Autism Spectrum Disorder? A Systematic Review and Meta-Analysis. In: Journal of the American Academy of Child and Adolescent Psychiatry, vol. 56. Elsevier Inc.; 2017. p. 466–74.
75.
go back to reference Ferreira H, Sousa AC, Sereno J, Martins J, Castelo-Branco M, Gonçalves J. Sex-Dependent Social and Repetitive Behavior and Neurochemical Profile in Mouse Model of Autism Spectrum Disorder. Metabolites. 2022;12(1) Ferreira H, Sousa AC, Sereno J, Martins J, Castelo-Branco M, Gonçalves J. Sex-Dependent Social and Repetitive Behavior and Neurochemical Profile in Mouse Model of Autism Spectrum Disorder. Metabolites. 2022;12(1)
77.
go back to reference Maximo JO, Cadena EJ, Kana RK. The implications of brain connectivity in the neuropsychology of autism. Neuropsychol Rev. 2014;24:16–31. Maximo JO, Cadena EJ, Kana RK. The implications of brain connectivity in the neuropsychology of autism. Neuropsychol Rev. 2014;24:16–31.
Metadata
Title
Neurofeedback training of executive function in autism spectrum disorder: distinct effects on brain activity levels and compensatory connectivity changes
Authors
Daniela Jardim Pereira
Sofia Morais
Alexandre Sayal
João Pereira
Sofia Meneses
Graça Areias
Bruno Direito
António Macedo
Miguel Castelo-Branco
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Journal of Neurodevelopmental Disorders / Issue 1/2024
Print ISSN: 1866-1947
Electronic ISSN: 1866-1955
DOI
https://doi.org/10.1186/s11689-024-09531-2

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