Differential Neural Mechanisms of Feedback Processing in Children with Developmental Language Disorder: An Examination of Midfrontal Theta Connectivity
Abstract
:1. Introduction
2. Materials and Methods
2.1. Subjects
2.2. Task Procedure
2.3. Statistical Analyses
Behavioral Analyses
2.4. EEG Data Acquisition and Processing
2.4.1. Time–Frequency Analysis
2.4.2. Connectivity Analysis
3. Results
3.1. Behavioral Results
3.2. Midfrontal Theta ITC Results
3.2.1. Effective Feedback: Between Groups Comparison of Theta ITC
3.2.2. Effective vs. Ineffective Feedback Processing in Children with DLD: Within-Group (DLD) Evaluation of Theta ITC
3.2.3. Connectivity between Sites during Feedback Processing: Theta Phase-Locking Value (PLV) Measures
Effective Feedback: A Between-Group (TD, DLD) Comparison
Effective and Ineffective Feedback: Within-Group Comparison (DLD Only)
3.2.4. Lateralization Effect of Theta PLV Measures
Effective Feedback: Between-Group (TD and DLD) Comparison
Effective and Ineffective Feedback: Within-Group Comparison (DLD Only)
4. Discussion
4.1. Effective and Ineffective Feedback Processing in the DLD Group
4.2. Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Arbel, Y.; Fitzpatrick, I.; He, X. Learning with and Without Feedback in Children with Developmental Language Disorder. J. Speech Lang. Hear. Res. 2021, 64, 1696–1711. [Google Scholar] [CrossRef] [PubMed]
- Gul, A.; Baron, L.; Arbel, Y. Feedback Processing During Probabilistic Learning in Children with Developmental Language Disorder: An Event-Related Potential Study. J. Speech Lang. Hear. Res. 2022, 65, 2272–2287. [Google Scholar] [CrossRef] [PubMed]
- Holroyd, C.B.; Coles, M.G.H. The Neural Basis of Human Error Processing: Reinforcement Learning, Dopamine, and the Error-Related Negativity. Psychol. Rev. 2002, 109, 679–709. [Google Scholar] [CrossRef] [PubMed]
- Cohen, M.X.; Cavanagh, J.F.; Slagter, H.A. Event-Related Potential Activity in the Basal Ganglia Differentiates Rewards from Nonrewards: Temporospatial Principal Components Analysis and Source Localization of the Feedback Negativity: Commentary. Hum. Brain Mapp. 2011, 32, 2270–2271. [Google Scholar] [CrossRef] [PubMed]
- Cohen, M.X.; Ranganath, C. Reinforcement Learning Signals Predict Future Decisions. J. Neurosci. 2007, 27, 371–378. [Google Scholar] [CrossRef]
- Müller, S.V.; Möller, J.; Rodriguez-Fornells, A.; Münte, T.F. Brain Potentials Related to Self-Generated and External Information Used for Performance Monitoring. Clin. Neurophysiol. 2005, 116, 63–74. [Google Scholar] [CrossRef]
- Cohen, M.X.; Donner, T.H. Midfrontal Conflict-Related Theta-Band Power Reflects Neural Oscillations That Predict Behavior. J. Neurophysiol. 2013, 110, 2752–2763. [Google Scholar] [CrossRef]
- Stuss, D.T.; Knight, R.T. Principles of Frontal Lobe Function; Oxford University Press: Oxford, UK, 2002. [Google Scholar]
- Amiez, C.; Hadj-Bouziane, F.; Petrides, M. Response Selection versus Feedback Analysis in Conditional Visuo-Motor Learning. NeuroImage 2012, 59, 3723–3735. [Google Scholar] [CrossRef]
- Cohen, M.X.; Wilmes, K.A.; Van De Vijver, I. Cortical Electrophysiological Network Dynamics of Feedback Learning. Trends Cogn. Sci. 2011, 15, 558–566. [Google Scholar] [CrossRef]
- Jobson, D.D.; Hase, Y.; Clarkson, A.N.; Kalaria, R.N. The Role of the Medial Prefrontal Cortex in Cognition, Ageing and Dementia. Brain Commun. 2021, 3, fcab125. [Google Scholar] [CrossRef]
- Cavanagh, J.F.; Frank, M.J. Frontal Theta as a Mechanism for Cognitive Control. Trends Cogn. Sci. 2014, 18, 414–421. [Google Scholar] [CrossRef] [PubMed]
- Cohen, M.X. Midfrontal Theta Tracks Action Monitoring over Multiple Interactive Time Scales. NeuroImage 2016, 141, 262–272. [Google Scholar] [CrossRef] [PubMed]
- Andreou, C.; Frielinghaus, H.; Rauh, J.; Mußmann, M.; Vauth, S.; Braun, P.; Leicht, G.; Mulert, C. Theta and High-Beta Networks for Feedback Processing: A Simultaneous EEG–fMRI Study in Healthy Male Subjects. Transl. Psychiatry 2017, 7, e1016. [Google Scholar] [CrossRef] [PubMed]
- Cunillera, T.; Fuentemilla, L.; Periañez, J.; Marco-Pallarès, J.; Krämer, U.M.; Càmara, E.; Münte, T.F.; Rodríguez-Fornells, A. Brain Oscillatory Activity Associated with Task Switching and Feedback Processing. Cogn. Affect. Behav. Neurosci. 2012, 12, 16–33. [Google Scholar] [CrossRef]
- Luft, C.D.B.; Nolte, G.; Bhattacharya, J. High-Learners Present Larger Mid-Frontal Theta Power and Connectivity in Response to Incorrect Performance Feedback. J. Neurosci. 2013, 33, 2029–2038. [Google Scholar] [CrossRef]
- van de Vijver, I.; Ridderinkhof, K.R.; Cohen, M.X. Frontal Oscillatory Dynamics Predict Feedback Learning and Action Adjustment. J. Cogn. Neurosci. 2011, 23, 4106–4121. [Google Scholar] [CrossRef]
- Van Noordt, S.; Wu, J.; Venkataraman, A.; Larson, M.J.; South, M.; Crowley, M.J. Inter-Trial Coherence of Medial Frontal Theta Oscillations Linked to Differential Feedback Processing in Youth and Young Adults with Autism. Res. Autism Spectr. Disord. 2017, 37, 1–10. [Google Scholar] [CrossRef]
- Shafritz, K.M.; Dichter, G.S.; Baranek, G.T.; Belger, A. The Neural Circuitry Mediating Shifts in Behavioral Response and Cognitive Set in Autism. Biol. Psychiatry 2008, 63, 974–980. [Google Scholar] [CrossRef]
- Yeung, M.K.; Han, Y.M.Y.; Sze, S.L.; Chan, A.S. Abnormal Frontal Theta Oscillations Underlie the Cognitive Flexibility Deficits in Children with High-Functioning Autism Spectrum Disorders. Neuropsychology 2016, 30, 281–295. [Google Scholar] [CrossRef]
- Fries, P. Rhythms for Cognition: Communication through Coherence. Neuron 2015, 88, 220–235. [Google Scholar] [CrossRef]
- Fries, P. A Mechanism for Cognitive Dynamics: Neuronal Communication through Neuronal Coherence. Trends Cogn. Sci. 2005, 9, 474–480. [Google Scholar] [CrossRef] [PubMed]
- Cavanagh, J.F.; Cohen, M.X.; Allen, J.J.B. Prelude to and Resolution of an Error: EEG Phase Synchrony Reveals Cognitive Control Dynamics during Action Monitoring. J. Neurosci. 2009, 29, 98–105. [Google Scholar] [CrossRef] [PubMed]
- Cavanagh, J.F.; Frank, M.J.; Klein, T.J.; Allen, J.J.B. Frontal Theta Links Prediction Errors to Behavioral Adaptation in Reinforcement Learning. NeuroImage 2010, 49, 3198–3209. [Google Scholar] [CrossRef] [PubMed]
- Ridderinkhof, K.R.; Van Den Wildenberg, W.P.M.; Segalowitz, S.J.; Carter, C.S. Neurocognitive Mechanisms of Cognitive Control: The Role of Prefrontal Cortex in Action Selection, Response Inhibition, Performance Monitoring, and Reward-Based Learning. Brain Cogn. 2004, 56, 129–140. [Google Scholar] [CrossRef]
- Kaufman Brief Intelligence Test. Second Edition. Available online: https://www.pearsonassessments.com/store/usassessments/en/Store/Professional-Assessments/Cognition-%26-Neuro/Kaufman-Brief-Intelligence-Test-%7C-Second-Edition/p/100000390.html (accessed on 7 March 2024).
- Obeid, J.S.; McGraw, C.A.; Minor, B.L.; Conde, J.G.; Pawluk, R.; Lin, M.; Wang, J.; Banks, S.R.; Hemphill, S.A.; Taylor, R.; et al. Procurement of Shared Data Instruments for Research Electronic Data Capture (REDCap). J. Biomed. Inform. 2013, 46, 259–265. [Google Scholar] [CrossRef]
- Mailend, M.L.; Plante, E.; Anderson, M.A.; Applegate, E.B.; Nelson, N.W. Reliability of the Test of Integrated Language and Literacy Skills (TILLS). Int. J. Lang. Commun. Disord. 2016, 51, 447–459. [Google Scholar] [CrossRef]
- Kapa, L.L.; Plante, E. Executive Function in SLI: Recent Advances and Future Directions. Curr. Dev. Disord. Rep. 2015, 2, 245–252. [Google Scholar] [CrossRef]
- Gooch, D.; Thompson, P.; Nash, H.M.; Snowling, M.J.; Hulme, C. The Development of Executive Function and Language Skills in the Early School Years. J. Child Psychol. Psychiatry 2016, 57, 180–187. [Google Scholar] [CrossRef]
- Henry, L.A.; Messer, D.J.; Nash, G. Executive Functioning in Children with Specific Language Impairment. J. Child Psychol. Psychiatry 2012, 53, 37–45. [Google Scholar] [CrossRef]
- Marton, K. Visuo-spatial Processing and Executive Functions in Children with Specific Language Impairment. Int. J. Lang. Commun. Disord. 2008, 43, 181–200. [Google Scholar] [CrossRef]
- Aljahlan, Y.; Spaulding, T.J. Attentional Shifting in Children with Developmental Language Disorder: A Meta-Analysis. J. Commun. Disord. 2021, 91, 106105. [Google Scholar] [CrossRef] [PubMed]
- Cavanagh, J.F.; Zambrano-Vazquez, L.; Allen, J.J.B. Theta Lingua Franca: A Common Mid-frontal Substrate for Action Monitoring Processes. Psychophysiology 2012, 49, 220–238. [Google Scholar] [CrossRef] [PubMed]
- Cavanagh, J.F. Cortical Delta Activity Reflects Reward Prediction Error and Related Behavioral Adjustments, but at Different Times. NeuroImage 2015, 110, 205–216. [Google Scholar] [CrossRef] [PubMed]
- Gul, A.; Baron, L.S.; Arbel, Y. The Contribution of Theta and Delta to Feedback Processing in Children with Developmental Language Disorder. J. Neurodev. Disord. 2023, 15, 13. [Google Scholar] [CrossRef]
- Lachaux, J.-P.; Rodriguez, E.; Martinerie, J.; Varela, F.J. Measuring Phase Synchrony in Brain Signals. Hum. Brain Mapp. 1999, 8, 194–208. [Google Scholar] [CrossRef]
- Ferdinand, N.K.; Becker, A.M.W.; Kray, J.; Gehring, W.J. Feedback Processing in Children and Adolescents: Is There a Sensitivity for Processing Rewarding Feedback? Neuropsychologia 2016, 82, 31–38. [Google Scholar] [CrossRef]
- Arbel, Y.; Wu, H. A Neurophysiological Examination of Quality of Learning in a Feedback-Based Learning Task. Neuropsychologia 2016, 93, 13–20. [Google Scholar] [CrossRef]
- Giandomenico, K.; Baron, L.S.; Gul, A.; Arbel, Y. Between Shifting and Feedback Processing in the Wisconsin Card Sorting Test in Children with Developmental Language Disorder. Brain Sci. 2023, 13, 1128. [Google Scholar] [CrossRef]
- Schneider, W.; Eschman, A.; Zuccolotto, A. E-Prime; Psychology Software Tools Inc.: Pittsburgh, PA, USA, 2002. [Google Scholar]
- Delorme, A.; Makeig, S. EEGLAB: An Open Source Toolbox for Analysis of Single-Trial EEG Dynamics Including Independent Component Analysis. J. Neurosci. Methods 2004, 134, 9–21. [Google Scholar] [CrossRef]
- The MathWorks, Inc. MATLAB 2022; MathWorks: Natick, MA, USA, 2022. [Google Scholar]
- Winkler, I.; Debener, S.; Müller, K.-R.; Tangermann, M. On the Influence of High-Pass Filtering on ICA-Based Artifact Reduction in EEG-ERP. In Proceedings of the 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC), Milan, Italy, 25–29 August 2015. [Google Scholar] [CrossRef]
- Palmer, J.A.; Kreutz-Delgado, K.; Makeig, S. AMICA: An Adaptive Mixture of Independent Component Analyzers with Shared Components. In Swartz Center for Computatonal Neursoscience; University of California San Diego: La Jolla, CA, USA, 2011. [Google Scholar]
- Namburi, P. Phase Locking Value. 2011. Available online: https://praneethnamburi.com/2011/08/10/plv/ (accessed on 27 February 2024).
- Rusjan, P.M.; Barr, M.S.; Farzan, F.; Arenovich, T.; Maller, J.J.; Fitzgerald, P.B.; Daskalakis, Z.J. Optimal Transcranial Magnetic Stimulation Coil Placement for Targeting the Dorsolateral Prefrontal Cortex Using Novel Magnetic Resonance Image-guided Neuronavigation. Hum. Brain Mapp. 2010, 31, 1643–1652. [Google Scholar] [CrossRef]
- Gul, A.; Baron, L.S.; Black, K.B.; Schafer, A.L.; Arbel, Y. Declarative Learning Mechanisms Support Declarative but Not Probabilistic Feedback-Based Learning in Children with Developmental Language Disorder (DLD). Brain Sci. 2023, 13, 1649. [Google Scholar] [CrossRef] [PubMed]
- West, R.; Bailey, K.; Tiernan, B.N.; Boonsuk, W.; Gilbert, S. The Temporal Dynamics of Medial and Lateral Frontal Neural Activity Related to Proactive Cognitive Control. Neuropsychologia 2012, 50, 3450–3460. [Google Scholar] [CrossRef] [PubMed]
- Missonnier, P.; Deiber, M.-P.; Gold, G.; Millet, P.; Gex-Fabry Pun, M.; Fazio-Costa, L.; Giannakopoulos, P.; Ibáñez, V. Frontal Theta Event-Related Synchronization: Comparison of Directed Attention and Working Memory Load Effects. J. Neural Transm. 2006, 113, 1477–1486. [Google Scholar] [CrossRef] [PubMed]
- West, R.; Huet, A. The Effect of Aging on the ERP Correlates of Feedback Processing in the Probabilistic Selection Task. Brain Sci. 2020, 10, 40. [Google Scholar] [CrossRef] [PubMed]
- Rushworth, M.F.S.; Behrens, T.E.J. Choice, Uncertainty and Value in Prefrontal and Cingulate Cortex. Nat. Neurosci. 2008, 11, 389–397. [Google Scholar] [CrossRef]
- Botvinick, M.M.; Carter, C.S.; Braver, T.S.; Barch, D.M.; Cohen, J.D. Conflict Monitoring and Cognitive Control. Psychol. Rev. 2001, 108, 624. [Google Scholar] [CrossRef]
- Botvinick, M.M. Conflict Monitoring and Decision Making: Reconciling Two Perspectives on Anterior Cingulate Function. Cogn. Affect. Behav. Neurosci. 2007, 7, 356–366. [Google Scholar] [CrossRef]
- Crone, E.A.; Donohue, S.E.; Honomichl, R.; Wendelken, C.; Bunge, S.A. Brain Regions Mediating Flexible Rule Use during Development. J. Neurosci. 2006, 26, 11239–11247. [Google Scholar] [CrossRef]
- Crone, E.A.; Wendelken, C.; Donohue, S.E.; Bunge, S.A. Neural Evidence for Dissociable Components of Task-Switching. Cereb. Cortex 2006, 16, 475–486. [Google Scholar] [CrossRef]
TD | DLD | One-Way ANOVA Results | |||
---|---|---|---|---|---|
Inclusionary Measure | n = 17 | n = 16 | Df | F | p |
Age (months) | 112.47 (9.65) | 112.69 (12.91) | 1, 31 | 0.003 | 0.957 |
KBIT-2 Matrices Score | 116.12 (13.89) | 102.38 (14.31) | 1, 31 | 7.83 | 0.009 |
TILLS Identification Core Score | 44.47 (5.73) | 23.81 (6.19) | 1, 31 | 99.07 | <0.000 |
TILLS Identification Core Score (Standard Score) | 107.65 (9.99) | 71.56 (10.75) | 1, 31 | 99.92 | <0.000 |
Chi-Squared Test Results | |||||
Sex: | Df | Χ2 | p | ||
Female | 8 | 7 | 1, n = 33 | 0.036 | 0.849 |
Male | 9 | 9 |
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Gul, A.; Schafer, A.L.; Arbel, Y. Differential Neural Mechanisms of Feedback Processing in Children with Developmental Language Disorder: An Examination of Midfrontal Theta Connectivity. Children 2024, 11, 1221. https://doi.org/10.3390/children11101221
Gul A, Schafer AL, Arbel Y. Differential Neural Mechanisms of Feedback Processing in Children with Developmental Language Disorder: An Examination of Midfrontal Theta Connectivity. Children. 2024; 11(10):1221. https://doi.org/10.3390/children11101221
Chicago/Turabian StyleGul, Asiya, Annika L. Schafer, and Yael Arbel. 2024. "Differential Neural Mechanisms of Feedback Processing in Children with Developmental Language Disorder: An Examination of Midfrontal Theta Connectivity" Children 11, no. 10: 1221. https://doi.org/10.3390/children11101221
APA StyleGul, A., Schafer, A. L., & Arbel, Y. (2024). Differential Neural Mechanisms of Feedback Processing in Children with Developmental Language Disorder: An Examination of Midfrontal Theta Connectivity. Children, 11(10), 1221. https://doi.org/10.3390/children11101221