Skip to main content

Advertisement

Log in

A stacked sparse auto-encoder and back propagation network model for sensory event detection via a flexible ECoG

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

Abstract

Current prostheses are limited in their ability to provide direct sensory feedback to users with missing limb. Several efforts have been made to restore tactile sensation to amputees but the somatotopic tactile feedback often results in unnatural sensations, and it is yet unclear how and what information the somatosensory system receives during voluntary movement. The present study proposes an efficient model of stacked sparse autoencoder and back propagation neural network for detecting sensory events from a highly flexible electrocorticography (ECoG) electrode. During the mechanical stimulation with Von Frey (VF) filament on the plantar surface of rats’ foot, simultaneous recordings of tactile afferent signals were obtained from primary somatosensory cortex (S1) in the brain. In order to achieve a model with optimal performance, Particle Swarm Optimization and Adaptive Moment Estimation (Adam) were adopted to select the appropriate number of neurons, hidden layers and learning rate of each sparse auto-encoder. We evaluated the stimulus-evoked sensation by using an automated up-down (UD) method otherwise called UDReader. The assessment of tactile thresholds with VF shows that the right side of the hind-paw was significantly more sensitive at the tibia-(p = 6.50 × 10−4), followed by the saphenous-(p = 7.84 × 10−4), and sural-(p = 8.24 × 10−4). We then validated our proposed model by comparing with the state-of-the-art methods, and recorded accuracy of 98.8%, sensitivity of 96.8%, and specificity of 99.1%. Hence, we demonstrated the effectiveness of our algorithms in detecting sensory events through flexible ECoG recordings which could be a viable option in restoring somatosensory feedback.

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
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Antfolk C, D’Alonzo M, Rosén B, Lundborg G, Sebelius F, Cipriani C (2013) Sensory feedback in upper limb prosthetics. Expert Rev Med Devices 10(1):45–54

    Article  CAS  Google Scholar 

  • Azlan WAW, Low YF (2014) Feature extraction of electroencephalogram (EEG) signal—a review. In: 2014 IEEE conference on biomedical engineering and sciences (IECBES), Kuala Lumpur, pp 801–806

  • Bernarding C, Strauss DJ, Hannemann R et al (2017) Neurodynamic evaluation of hearing aid features using EEG correlates of listening effort. Cogn Neurodyn 11:203–215

    Article  Google Scholar 

  • Bonin RP, Bories C, Koninck YD (2014) A simplified up-down method (SUDO) for measuring mechanical nociception in rodents using von Frey filaments. Mol Pain 10:26. https://doi.org/10.1186/1744-8069-10-26

    Article  PubMed  PubMed Central  Google Scholar 

  • Caldwell DJ, Ojemann JG, Rao RPN (2019) Direct electrical stimulation in electrocorticographic brain–computer interfaces: enabling technologies for input to cortex. Front Neurosci 13:804

    Article  Google Scholar 

  • Caro-Martín CR, Delgado-García JM, Gruart A, Sánchez-Campusano R (2018) Spike sorting based on shape, phase, and distribution features, and K-TOPS clustering with validity and error indices. Sci Rep 8:17796. https://doi.org/10.1038/s41598-018-35491-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55–63

    Article  CAS  Google Scholar 

  • Chen G (2014) Automatic EEG seizure detection using dual-tree complex wavelet-Fourier features. Expert Syst Appl 41(5):2391–2394

    Article  Google Scholar 

  • Choi I, Rhiu I, Lee Y, Yun MH, Nam CS (2017) A systematic review of hybrid brain-computer interfaces: taxonomy and usability perspectives. PLoS ONE. https://doi.org/10.1371/journal.pone.0176674

    Article  PubMed  PubMed Central  Google Scholar 

  • Cordella F, Ciancio AL, Sacchetti R, Davalli A, Cutti AG, Guglielmelli E, Zollo L (2016) Literature review on needs of upper limb prosthesis users. Front Neurosci 10:209

    Article  Google Scholar 

  • Cronin JA et al (2016) Task-specific somatosensory feedback via cortical stimulation in humans. IEEE Trans Haptics 9(4):515–522. https://doi.org/10.1109/toh.2016.2591952

    Article  PubMed  PubMed Central  Google Scholar 

  • Daoud H, Bayoumi MA (2019) Efficient epileptic seizure prediction based on deep learning. IEEE Trans Biomed Circuits Syst 13(5):804–813

    Article  Google Scholar 

  • Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441–462

    Article  CAS  Google Scholar 

  • Fang P et al (2015) New control strategies for multifunctional prostheses that combine electromyographic and speech signals. IEEE Intell Syst 30(04):47–53. https://doi.org/10.1109/MIS.2015.40

    Article  Google Scholar 

  • Flesher N, Collinger L, Foldes T, Weiss M, Downey E, Tyler-Kabara C, Bensmaia J, Schwartz B, Boninger L, Gaunt A (2016) Intracortical microstimulation of human somatosensory cortex. Sci Transl Med 8(361):361ra141

    Article  Google Scholar 

  • González-Cano R, Boivin B, Bullock D, Cornelissen L, Andrews NA, Costigan ML (2018) Up–down reader: an open source program for efficiently processing 50% von Frey thresholds. Front Pharmacol 9:433

    Article  Google Scholar 

  • Hatsopoulos NG, Donoghue JP (2009) The science of neural interface systems. Annu Rev Neurosci 32:249–266

    Article  CAS  Google Scholar 

  • Hill NJ, Gupta D, Brunner P, Gunduz A, Adamo MA, Ritaccio A, Schalk G (2012) Recording human electrocorticographic (ECoG) signals for neuroscientific research and real-time functional cortical mapping. J Vis Exp JoVE 64:3993. https://doi.org/10.3791/3993

    Article  Google Scholar 

  • Hinton GE, Salakhutdinov RR (2006) Reducing the dimensionality of data with neural networks. Science 313(5786):504–507

    Article  CAS  Google Scholar 

  • Hiremath SV, Tyler-Kabara EC, Wheeler JJ, Moran DW, Gaunt RA, Collinger JL et al (2017) Human perception of electrical stimulation on the surface of somatosensory cortex. PLoS ONE 12(5):e0176020. https://doi.org/10.1371/journal.pone.0176020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Idowu, O.P., Fang, P., Li, X., Xia, Z., Xiong, J., & Li, G. (2018). Towards control of EEG-based robotic arm using deep learning via stacked sparse autoencoder. In: IEEE international conference on robotics and biomimetics (ROBIO), pp 1053–1057

  • Idowu OP, Huang J, Zhao Y, Li G, Fang P (2018b) Electrophysiological assessment of peripheral nerve stimulation through somatosensory evoked potential in rat hindlimb. IEEE Int Conf Cyborg Bionic Syst (CBS) 2018:21–24

    Google Scholar 

  • Kaiju T, Doi K, Yokota M, Watanabe K, Inoue M, Ando H, Takahashi K, Yoshida F, Hirata M, Suzuki T (2017) High spatiotemporal resolution ECoG recording of somatosensory evoked potentials with flexible micro-electrode arrays. Front Neural Circuits 11:20

    Article  Google Scholar 

  • Kim GH, Kim K, Lee E, An T, Choi W, Lim G, Shin JH (2018) Recent progress on microelectrodes in neural interfaces. Materials (Basel, Switzerland) 11(10):1995

    Article  Google Scholar 

  • Kingma DP, Ba J (2014). Adam: a method for stochastic optimization. CoRR, abs/1412.6980

  • Lambert GA, Mallos G, Zagami AS (2009) Von Frey’s hairs—a review of their technology and use—a novel automated von Frey device for improved testing for hyperalgesia. J Neurosci Methods 177:420–426

    Article  Google Scholar 

  • Lefebvre B, Yger P, Marre O (2016) Recent progress in multi-electrode spike sorting methods. J Physiol Paris 110(4 Pt A):327–335

    Article  Google Scholar 

  • Li G, Samuel OW, Lin C, Asogbon MG, Fang P, Idowu PO (2019) Realizing efficient EMG-based prosthetic control strategy. Adv Exp Med Biol 1101:149–166. ISSN: 0065-2598

  • Meisel C, Bailey KA (2019) Identifying signal-dependent information about the preictal state: a comparison across ECoG, EEG and EKG using deep learning. EBioMedicine 45:422–431. https://doi.org/10.1016/j.ebiom.2019.07.001

    Article  PubMed  PubMed Central  Google Scholar 

  • Mohammadpoory Z, Nasrolahzadeh M, Mahmoodian N et al (2019) Complex network based models of ECoG signals for detection of induced epileptic seizures in rats. Cogn Neurodyn 13:325–339. https://doi.org/10.1007/s11571-019-09527-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Mora-Sánchez A, Dreyfus G, Vialatte F (2019) Scale-free behaviour and metastable brain-state switching driven by human cognition, an empirical approach. Cogn Neurodyn 13:437–452. https://doi.org/10.1007/s11571-019-09533-0

    Article  PubMed  Google Scholar 

  • Nedic A, Moon JD, Kung TA, Langhals NB, Cederna PS, Urbanchek MG (2013) Von Frey monofilament testing successfully discriminates between sensory function of mixed nerve and sensory nerve regenerative peripheral nerve interfaces. In: 2013 6th International IEEE/EMBS conference on neural engineering (NER), pp 255–258

  • Niknazar M, Mousavi SR, Motaghi S, Dehghani A, Vosoughi Vahdat B, Shamsollahi MB, Sayyah M, Noorbakhsh SM (2013) A unified approach for detection of induced epileptic seizures in rats using ECoG signals. Epilepsy Behav 27(2):355–364

    Article  CAS  Google Scholar 

  • Obien ME, Deligkaris K, Bullmann T, Bakkum DJ, Frey U (2015) Revealing neuronal function through microelectrode array recordings. Front Neurosci 8:423

    Article  Google Scholar 

  • Rahman MA, Ma W, Tran D, Campbell J (2012) A comprehensive survey of the feature extraction methods in the EEG research. ICA3PP

  • Randall JN (1996) Interactions between motor commands and somatic perception in sensorimotor cortex. Curr Opin Neurobiol 6:801–810

    Article  Google Scholar 

  • Rao AR (2018) An oscillatory neural network model that demonstrates the benefits of multisensory learning. Cogn Neurodyn 12:481–499. https://doi.org/10.1007/s11571-018-9489-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Raspopovic S, Carpaneto J, Udina E, Navarro X, Micera S (2010) On the identification of sensory information from mixed nerves by using single-channel cuff electrodes. J NeuroEng Rehabil 7:17. https://doi.org/10.1186/1743-0003-7-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Ravish DK, Shenbaga Devi S, Krishnamoorthy SG, Karthikeyan MR (2013) Detection of epileptic seizure in eeg recordings by spectral method and statistical analysis. J Appl Sci 13:207–219

    Article  Google Scholar 

  • Rey HG, Pedreira C, Quiroga RQ (2015) Past, present and future of spike sorting techniques. Brain Res Bull 119:106–117

    Article  Google Scholar 

  • Roberts JA, Gollo LL, Abeysuriya RG et al (2019) Metastable brain waves. Nat Commun 10:1056. https://doi.org/10.1038/s41467-019-08999-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy Y, Banville HJ, Albuquerque I, Gramfort A, Falk TH, Faubert J (2019) Deep learning-based electroencephalography analysis: a systematic review. J Neural Eng 16(5):051001. https://doi.org/10.1088/1741-2552/ab260c

    Article  PubMed  Google Scholar 

  • Samuel OW, Geng Y, Li X, Li G (2017) Towards efficient decoding of multiple classes of motor imagery limb movements based on EEG spectral and time domain descriptors. J Med Syst 41(12):194

    Article  Google Scholar 

  • Schiefer M, Tan D, Sidek SM et al (2016) Sensory feedback by peripheral nerve stimulation improves task performance in individuals with upper limb loss using a myoelectric prosthesis. J Neural Eng 13(1):016001

    Article  Google Scholar 

  • Sharmila A, Mahalakshmi P (2017) Wavelet-based feature extraction for classification of epileptic seizure EEG signal. J Med Eng Technol 41(8):670–680. https://doi.org/10.1080/03091902.2017.1394388

    Article  CAS  PubMed  Google Scholar 

  • Shi Y (2001) Particle swarm optimization: developments, applications and resources. In: Proceedings of the 2001 congress on evolutionary computation (IEEE Cat. No.01TH8546), vol 1, pp 81–86

  • Stephens-Fripp B, Alici G, Mutlu R (2018) A review of non-invasive sensory feedback methods for transradial prosthetic hands. IEEE Access 6:6878–6899

    Article  Google Scholar 

  • Svensson P, Wijk U, Björkman A, Antfolk C (2017) A review of invasive and non-invasive sensory feedback in upper limb prostheses. Expert Rev Med Devices 14(6):439–447

    Article  CAS  Google Scholar 

  • Thakor NV (2013) Translating the brain-machine interface. Sci Transl Med 5(210):210ps17

    Article  Google Scholar 

  • Umeda T, Isa T, Nishimura Y (2019) The somatosensory cortex receives information about motor output. Sci Adv 5(7):eaaw5388. https://doi.org/10.1126/sciadv.aaw5388

    Article  PubMed  PubMed Central  Google Scholar 

  • Volkova K, Lebedev MA, Kaplan A, Ossadtchi A (2019) Decoding movement from electrocorticographic activity: a review. Front Neuroinf 13:74

    Article  Google Scholar 

  • Waldert S (2016) Invasive vs. non-invasive neuronal signals for brain-machine interfaces: will one prevail? Front Neurosci 10:295. https://doi.org/10.3389/fnins.2016.00295

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang C, Zou J, Zhang J, Wang M, Wang R (2010) Feature extraction and recognition of epileptiform activity in EEG by combining PCA with ApEn. Cogn Neurodyn 4(3):233–240. https://doi.org/10.1007/s11571-010-9120-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang D, Liu Y, Hu D, Blohm G (2015a) EEG-based perceived tactile location prediction. IEEE Trans Auton Ment Dev 7:342–348

    Article  Google Scholar 

  • Wang R, Wang J, Yu H, Wei X, Yang C, Deng B (2015b) Power spectral density and coherence analysis of Alzheimer’s EEG. Cogn Neurodyn 9(3):291–304. https://doi.org/10.1007/s11571-014-9325-x

    Article  PubMed  Google Scholar 

  • Zhao Y, Yu M, Li G, Fang P (2018) Highly stretchable electrodes based on gold films with cyclic stability for electrocorticogram recordings. IEEE Int Conf Cyborg Bionic Syst (CBS) 2018:17–20

    Google Scholar 

Download references

Acknowledgements

This work was supported in part by the National Key Research & Development Program of China (2017YFA0701103), the Shenzhen Basic Research Program (JCYJ20170818163724754), the National Natural Science Foundation of China (61773364, 81927804 and U1613222), the CAS Youth Innovation Promotion Association (2018395), the Shenzhen Science and Technology Plan Project (JCYJ20160331174854880), and the Shenzhen Engineering Laboratory of Neural Rehabilitation Technology.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Peng Fang or Guanglin Li.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Idowu, O.P., Huang, J., Zhao, Y. et al. A stacked sparse auto-encoder and back propagation network model for sensory event detection via a flexible ECoG. Cogn Neurodyn 14, 591–607 (2020). https://doi.org/10.1007/s11571-020-09603-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-020-09603-8

Keywords

Navigation