Skip to main content
Log in

Brain state and dynamic transition patterns of motor imagery revealed by the bayes hidden markov model

  • Research Article
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

Abstract

Motor imagery (MI) is a high-level cognitive process that has been widely applied to brain-computer inference (BCI) and motor recovery. In practical applications, however, huge individual differences and unclear neural mechanisms have seriously hindered the application of MI and BCI systems. Thus, it is urgently needed to explore MI from a new perspective. Here, we applied a hidden Markov model (HMM) to explore the dynamic organization patterns of left- and right-hand MI tasks. Eleven distinct HMM states were identified based on MI-related EEG data. We found that these states can be divided into three metastates by clustering analysis, showing a highly organized structure. We also assessed the probability activation of each HMM state across time. The results showed that the state probability activation of task-evoked have similar trends to that of event-related desynchronization/synchronization (ERD/ERS). By comparing the differences in temporal features of HMM states between left- and right-hand MI, we found notable variations in fractional occupancy, mean life time, mean interval time, and transition probability matrix across stages and states. Interestingly, we found that HMM states activated in the left occipital lobe had higher occupancy during the left-hand MI task, and conversely, during the right-hand MI task, HMM states activated in the right occipital lobe had higher occupancy. Moreover, significant correlations were observed between BCI performance and features of HMM states. Taken together, our findings explored dynamic networks underlying the MI-related process and provided a complementary understanding of different MI tasks, which may contribute to improving the MI-BCI systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The data that support the findings of this study are openly available on the PhysioNet website (https://physionet.org).

References

  • Ahrends, C., Vidaurre, D. (2023) Predicting individual traits from models of brain dynamics accurately and reliably using the Fisher kernel. bioRxiv:530638.

  • Beauchamp MS (2015) The social mysteries of the superior temporal sulcus. Trends Cogn Sci 19:489–490

    Article  PubMed  PubMed Central  Google Scholar 

  • Bencivenga F, Sulpizio V, Tullo MG, Galati G (2021) Assessing the effective connectivity of premotor areas during real vs imagined grasping: a DCM-PEB approach. Neuroimage 230:117806

    Article  PubMed  Google Scholar 

  • Bishop CM, Nasrabadi NM (2006) Pattern recognition and machine learning. Springer

    Google Scholar 

  • Burianová H, Marstaller L, Sowman P, Tesan G, Rich AN, Williams M, Savage G, Johnson BW (2013) Multimodal functional imaging of motor imagery using a novel paradigm. Neuroimage 71:50–58

    Article  PubMed  Google Scholar 

  • Capotosto P, Tosoni A, Spadone S, Sestieri C, Perrucci MG, Romani GL, Della Penna S, Corbetta M (2013) Anatomical segregation of visual selection mechanisms in human parietal cortex. J Neurosci 33:6225–6229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho H, Ahn M, Ahn S, Kwon M, Jun SC (2017) EEG datasets for motor imagery brain–computer interface. GigaScience 6:gix034

    Article  Google Scholar 

  • Confalonieri L, Pagnoni G, Barsalou LW, Rajendra J, Eickhoff SB, Butler AJ. (2012) Brain activation in primary motor and somatosensory cortices during motor imagery correlates with motor imagery ability in stroke patients. International Scholarly Research Notices, 2012

  • Daeglau M, Zich C, Emkes R, Welzel J, Debener S, Kranczioch C (2020) Investigating priming effects of physical practice on motor imagery-induced event-related desynchronization. Front Psychol 11:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Decety J (1996) The neurophysiological basis of motor imagery. Behav Brain Res 77:45–52

    Article  CAS  PubMed  Google Scholar 

  • Duc NT, Lee B (2020) Decoding brain dynamics in speech perception based on EEG microstates decomposed by multivariate Gaussian hidden Markov model. IEEE Access 8:146770–146784

    Article  Google Scholar 

  • Eichenbaum H (2017) Prefrontal–hippocampal interactions in episodic memory. Nat Rev Neurosci 18:547–558

    Article  CAS  PubMed  Google Scholar 

  • Fadel W, Wahdow M, Kollod C, Marton G, Ulbert I (2020) Chessboard EEG images classification for BCI systems using deep neural network. Bio-inspired Information and Communication Technologies. In: 12th EAI International Conference,97–104

  • Fallgatter AJ, Mueller TJ, Strik WK (1997) Neurophysiological correlates of mental imagery in different sensory modalities. Int J Psychophysiol 25:145–153

    Article  CAS  PubMed  Google Scholar 

  • Gao Q, Duan X, Chen H (2011) Evaluation of effective connectivity of motor areas during motor imagery and execution using conditional Granger causality. Neuroimage 54:1280–1288

    Article  PubMed  Google Scholar 

  • Gao X, Wang Y, Chen X, Gao S (2021) Interface, interaction, and intelligence in generalized brain–computer interfaces. Trends Cogn Sci 25:671–684

    Article  PubMed  Google Scholar 

  • Goldberger AL, Amaral LA, Glass L, Hausdorff JM, Ivanov PC, Mark RG, Mietus JE, Moody GB, Peng C-K, Stanley HE (2000) PhysioBank, physiotoolkit, and physionet: components of a new research resource for complex physiologic signals. Circulation 101:e215–e220

    Article  CAS  PubMed  Google Scholar 

  • Guillot A, Di Rienzo F, Collet C (2014) The neurofunctional architecture of motor imagery. Advanced brain neuroimaging topics in health and disease-methods and applications, 433–456

  • Hétu S, Grégoire M, Saimpont A, Coll M-P, Eugène F, Michon P-E, Jackson PL (2013) The neural network of motor imagery: an ALE meta-analysis. Neurosci Biobehav Rev 37:930–949

    Article  PubMed  Google Scholar 

  • Hindriks R, Adhikari MH, Murayama Y, Ganzetti M, Mantini D, Logothetis NK, Deco G (2016) Can sliding-window correlations reveal dynamic functional connectivity in resting-state fMRI? Neuroimage 127:242–256

    Article  CAS  PubMed  Google Scholar 

  • Hunyadi B, Woolrich MW, Quinn AJ, Vidaurre D, De Vos M (2019) A dynamic system of brain networks revealed by fast transient EEG fluctuations and their fMRI correlates. Neuroimage 185:72–82

    Article  CAS  PubMed  Google Scholar 

  • Javaheripour N, Colic L, Opel N, Li M, Maleki Balajoo S, Chand T, Van der Meer J, Krylova M, Izyurov I, Meller T, Goltermann J, Winter NR, Meinert S, Grotegerd D, Jansen A, Alexander N, Usemann P, Thomas-Odenthal F, Evermann U, Wroblewski A, Brosch K, Stein F, Hahn T, Straube B, Krug A, Nenadić I, Kircher T, Croy I, Dannlowski U, Wagner G, Walter M (2023) Altered brain dynamic in major depressive disorder: state and trait features. Transl Psychiatry 13:261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang J-H, Jo YC, Kim S-P (2018) Electroencephalographic feature evaluation for improving personal authentication performance. Neurocomputing 287:93–101

    Article  Google Scholar 

  • Kang J-H, Youn J, Kim S-H, Kim J (2021) Effects of frontal theta rhythms in a prior resting state on the subsequent motor imagery brain-computer interface performance. Front Neurosci 15:663101

    Article  PubMed  PubMed Central  Google Scholar 

  • Khademi Z, Ebrahimi F, Kordy HM (2023) A review of critical challenges in MI-BCI: from conventional to deep learning methods. J Neurosci Methods 383:109736

    Article  PubMed  Google Scholar 

  • Khan MA, Das R, Iversen HK, Puthusserypady S (2020) Review on motor imagery based BCI systems for upper limb post-stroke neurorehabilitation: From designing to application. Comput Biol Med 123:103843

    Article  PubMed  Google Scholar 

  • Kiernan J (2012) Anatomy of the temporal lobe. Epilepsy research and treatment, 2012.

  • Kohli V, Tripathi U, Chamola V, Rout BK, Kanhere SS (2022) A review on virtual reality and augmented reality use-cases of brain computer interface based applications for smart cities. Microprocess Microsyst 88:104392

    Article  Google Scholar 

  • Lebon F, Horn U, Domin M, Lotze M (2018) Motor imagery training: kinesthetic imagery strategy and inferior parietal fMRI activation. Hum Brain Mapp 39:1805–1813

    Article  PubMed  PubMed Central  Google Scholar 

  • Lember J, Gasbarra D, Koloydenko A, Kuljus K (2019) Estimation of viterbi path in bayesian hidden Markov models. Metron 77:137–169

    Article  Google Scholar 

  • Li Y, Lei MY, Guo Y, Hu Z, Wei HL (2018) Time-varying nonlinear causality detection using regularized orthogonal least squares and multi-wavelets with applications to EEG. IEEE Access 6:17826–17840

    Article  Google Scholar 

  • Li F, Yi C, Song L, Jiang Y, Peng W, Si Y, Zhang T, Zhang R, Yao D, Zhang Y (2019) Brain network reconfiguration during motor imagery revealed by a large-scale network analysis of scalp EEG. Brain Topogr 32:304–314

    Article  PubMed  Google Scholar 

  • Li P, Li C, Bore JC, Si Y, Li F, Cao Z, Zhang Y, Wang G, Zhang Z, Yao D, Xu P (2022) L1-norm based time-varying brain neural network and its application to dynamic analysis for motor imagery. J Neural Eng 19:026019

    Article  Google Scholar 

  • Lin P, Zang S, Bai Y, Wang H (2022) Reconfiguration of brain network dynamics in autism spectrum disorder based on hidden markov model. Front Hum Neurosci 16:774921

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu K, Lai Q, Li P, Yu Z, Xiao B, Guan C, Wu W (2022) Robust bayesian estimation of eeg-based brain causality networks. In: IEEE transactions on biomedical engineering

  • Madan CR, Singhal A (2012) Motor imagery and higher-level cognition: four hurdles before research can sprint forward. Cogn Process 13:211–229

    Article  PubMed  Google Scholar 

  • Maruff P, Wilson PH, Fazio JD, Cerritelli B, Hedt A, Currie J (1999) Asymmetries between dominant and non-dominanthands in real and imagined motor task performance. Neuropsychologia 37:379–384

    Article  CAS  PubMed  Google Scholar 

  • Maya-Piedrahita MC, Herrera-Gomez PM, Berrío-Mesa L, Cárdenas-Peña DA, Orozco-Gutierrez AA (2022) Supported diagnosis of attention deficit and hyperactivity disorder from EEG based on interpretable kernels for hidden Markov models. Int J Neural Syst 32:2250008

    Article  CAS  PubMed  Google Scholar 

  • Milton J, Small SL, Solodkin A (2008) Imaging motor imagery: methodological issues related to expertise. Methods 45:336–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulder T, Zijlstra S, Zijlstra W, Hochstenbach J (2004) The role of motor imagery in learning a totally novel movement. Exp Brain Res 154:211–217

    Article  PubMed  Google Scholar 

  • Munzert J, Lorey B, Zentgraf K (2009) Cognitive motor processes: the role of motor imagery in the study of motor representations. Brain Res Rev 60:306–326

    Article  PubMed  Google Scholar 

  • Neuper, C., Pfurtscheller, G., Guillot, A., Collet, C. (2010) Electroencephalographic characteristics during motor imagery. The Neurophysiol Found Ment Mot Imag, 65–81

  • Nolde SF, Johnson MK, Raye CL (1998) The role of prefrontal cortex during tests of episodic memory. Trends Cogn Sci 2:399–406

    Article  CAS  PubMed  Google Scholar 

  • Ogawa T, Shimobayashi H, Hirayama J-I, Kawanabe M (2022) Asymmetric directed functional connectivity within the frontoparietal motor network during motor imagery and execution. Neuroimage 247:118794

    Article  PubMed  Google Scholar 

  • Olsson CJ, Nyberg L (2010) Motor imagery: if you can’t do it, you won’t think it. Scand J Med Sci Sports 20:711–715

    Article  PubMed  Google Scholar 

  • Parbat D, Chakraborty M (2021) A novel methodology to study the cognitive load induced EEG complexity changes: chaos, fractal and entropy based approach. Biomed Signal Process Control 64:102277

    Article  Google Scholar 

  • Pearson J (2019) The human imagination: the cognitive neuroscience of visual mental imagery. Nat Rev Neurosci 20:624–634

    Article  CAS  PubMed  Google Scholar 

  • Pearson J, Naselaris T, Holmes EA, Kosslyn SM (2015) Mental imagery: functional mechanisms and clinical applications. Trends Cogn Sci 19:590–602

    Article  PubMed  PubMed Central  Google Scholar 

  • Petrides M (2023) On the evolution of polysensory superior temporal sulcus and middle temporal gyrus: a key component of the semantic system in the human brain. J Comp Neurol 531:1987

    Article  PubMed  Google Scholar 

  • Pfurtscheller G, Neuper C (2006) Future prospects of ERD/ERS in the context of brain–computer interface (BCI) developments. Prog Brain Res 159:433–437

    Article  PubMed  Google Scholar 

  • Pilgramm S, de Haas B, Helm F, Zentgraf K, Stark R, Munzert J, Kruger B (2016) Motor imagery of hand actions: Decoding the content of motor imagery from brain activity in frontal and parietal motor areas. Hum Brain Mapp 37:81–93

    Article  PubMed  Google Scholar 

  • Quinn AJ, Vidaurre D, Abeysuriya R, Becker R, Nobre AC, Woolrich MW (2018) Task-evoked dynamic network analysis through hidden markov modeling. Front Neurosci 12:603

    Article  PubMed  PubMed Central  Google Scholar 

  • Rezek I, Roberts S (2005) Ensemble hidden Markov models with extended observation densities for biosignal analysis. Probabilistic modeling in bioinformatics and medical informatics. Springer, London, pp 419–450

    Chapter  Google Scholar 

  • Rolls ET, Deco G, Huang C-C, Feng J (2022) The effective connectivity of the human hippocampal memory system. Cereb Cortex 32:3706–3725

    Article  PubMed  Google Scholar 

  • Schalk G, McFarland DJ, Hinterberger T, Birbaumer N, Wolpaw JR (2004) BCI2000: a general-purpose brain-computer interface (BCI) system. IEEE Trans Biomed Eng 51:1034–1043

    Article  PubMed  Google Scholar 

  • Scolari M, Seidl-Rathkopf KN, Kastner S (2015) Functions of the human frontoparietal attention network: evidence from neuroimaging. Curr Opin Behav Sci 1:32–39

    Article  PubMed  Google Scholar 

  • Seedat ZA, Rier L, Gascoyne LE, Cook H, Woolrich MW, Quinn AJ, Roberts TP, Furlong PL, Armstrong C, St. Pier, K. (2023) Mapping interictal activity in epilepsy using a hidden markov model: a magnetoencephalography study. Hum Brain Mapp 44:66–81

    Article  PubMed  Google Scholar 

  • Slotnick SD, Thompson WL, Kosslyn SM (2012) Visual memory and visual mental imagery recruit common control and sensory regions of the brain. Cogn Neurosci 3:14–20

    Article  PubMed  Google Scholar 

  • Tacchino A, Saiote C, Brichetto G, Bommarito G, Roccatagliata L, Cordano C, Battaglia MA, Mancardi GL, Inglese M (2018) Motor imagery as a function of disease severity in multiple sclerosis: an fMRI study. Front Hum Neurosci 11:628

    Article  PubMed  PubMed Central  Google Scholar 

  • Talukdar U, Hazarika SM, Gan JQ (2020) Adaptation of common spatial patterns based on mental fatigue for motor-imagery BCI. Biomed Signal Process Control 58:101829

    Article  Google Scholar 

  • Tao Q, Si Y, Li F, Li P, Li Y, Zhang S, Wan F, Yao D, Xu P (2021) Decision-feedback stages revealed by hidden Markov modeling of EEG. Int J Neural Syst 31:2150031

    Article  PubMed  Google Scholar 

  • Van der Lubbe RH, Sobierajewicz J, Jongsma ML, Verwey WB, Przekoracka-Krawczyk A (2021) Frontal brain areas are more involved during motor imagery than during motor execution/preparation of a response sequence. Int J Psychophysiol 164:71–86

    Article  PubMed  Google Scholar 

  • Van Schependom J, Vidaurre D, Costers L, Sjøgård M, D’hooghe, M.B., D’haeseleer, M., Wens, V., De Tiège, X., Goldman, S., Woolrich, M. (2019) Altered transient brain dynamics in multiple sclerosis: treatment or pathology? Hum Brain Mapp 40:4789–4800

    Article  PubMed  PubMed Central  Google Scholar 

  • Vernon D, Beetz M, Sandini G (2015) Prospection in cognition: the case for joint episodic-procedural memory in cognitive robotics. Front Robot AI 2:19

    Article  Google Scholar 

  • Vidaurre D, Quinn AJ, Baker AP, Dupret D, Tejero-Cantero A, Woolrich MW (2016) Spectrally resolved fast transient brain states in electrophysiological data. Neuroimage 126:81–95

    Article  PubMed  Google Scholar 

  • Vidaurre D, Smith SM, Woolrich MW (2017) Brain network dynamics are hierarchically organized in time. Proc Natl Acad Sci 114:12827–12832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vidaurre D, Abeysuriya R, Becker R, Quinn AJ, Alfaro-Almagro F, Smith SM, Woolrich MW (2018a) Discovering dynamic brain networks from big data in rest and task. Neuroimage 180:646–656

    Article  PubMed  Google Scholar 

  • Vidaurre D, Hunt LT, Quinn AJ, Hunt BAE, Brookes MJ, Nobre AC, Woolrich MW (2018b) Spontaneous cortical activity transiently organises into frequency specific phase-coupling networks. Nat Commun 9:2987

    Article  PubMed  PubMed Central  Google Scholar 

  • Wei G, Luo J (2010) Sport expert’s motor imagery: functional imaging of professional motor skills and simple motor skills. Brain Res 1341:52–62

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Caprihan A, Calhoun V (2021) Tracking spatial dynamics of functional connectivity during a task. Neuroimage 239:118310

    Article  PubMed  Google Scholar 

  • Yang C, Ye Y, Li X, Wang R (2018) Development of a neuro-feedback game based on motor imagery EEG. Multimed Tools Appl 77:15929–15949

    Article  Google Scholar 

  • Yu H, Ba S, Guo Y, Guo L, Xu G (2022) Effects of motor imagery tasks on brain functional networks based on EEG Mu/Beta rhythm. Brain Sci 12:194

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Oh Y, Kounios J, Beeman M (2023) Uncovering the interplay of oscillatory processes during creative problem solving: a dynamic modeling approach. Creat Res J 35:438–454

    Article  PubMed  PubMed Central  Google Scholar 

  • Zapparoli L, Invernizzi P, Gandola M, Verardi M, Berlingeri M, Sberna M, De Santis A, Zerbi A, Banfi G, Bottini G, Paulesu E (2013) Mental images across the adult lifespan: a behavioural and fMRI investigation of motor execution and motor imagery. Exp Brain Res 224:519–540

    Article  CAS  PubMed  Google Scholar 

  • Zarghami TS, Friston KJ (2020) Dynamic effective connectivity. Neuroimage 207:116453

    Article  PubMed  Google Scholar 

  • Zarubin G, Gundlach C, Nikulin V, Villringer A, Bogdan M (2020) Transient amplitude modulation of alpha-band oscillations by short-time intermittent closed-loop tACS. Front Hum Neurosci 14:366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Liu T, Li F, Li M, Liu D, Zhang R, He H, Li P, Gong J, Luo C (2016) Structural and functional correlates of motor imagery BCI performance: insights from the patterns of fronto-parietal attention network. Neuroimage 134:475–485

    Article  PubMed  Google Scholar 

  • Zhang T, Li M, Zhang L, Biswal B, Yao D, Xu P (2018) The time-varying network patterns in motor imagery revealed by adaptive directed transfer function analysis for fMRI. IEEE Access 6:60339–60352

    Article  Google Scholar 

  • Zhang T, Wang F, Li M, Li F, Tan Y, Zhang Y, Yang H, Biswal B, Yao D, Xu P (2019) Reconfiguration patterns of large-scale brain networks in motor imagery. Brain Struct Funct 224:553–566

    Article  PubMed  Google Scholar 

  • Zhang S, Cao C, Quinn A, Vivekananda U, Zhan S, Liu W, Sun B, Woolrich M, Lu Q, Litvak V (2021) Dynamic analysis on simultaneous iEEG-MEG data via hidden Markov model. Neuroimage 233:117923

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (#62006197, #42305067), the project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (#SML2023SP203), Medical Science and Technology Research Fund of Guangdong Province (B2023186).

Author information

Authors and Affiliations

Authors

Contributions

YL: methodology, formal analysis, visualization, and writing. SY: data preprocessing and formal analysis. JL, JM, FW, and SS: data curation. DY and PX: Writing—review & editing. TZ: Funding acquisition, idea, Writing—review & editing.

Corresponding author

Correspondence to Tao Zhang.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 19 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Yu, S., Li, J. et al. Brain state and dynamic transition patterns of motor imagery revealed by the bayes hidden markov model. Cogn Neurodyn (2024). https://doi.org/10.1007/s11571-024-10099-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11571-024-10099-9

Keywords

Navigation