Abstract
Brain-machine interfaces (BMIs) have been widely used to study basic and translational neuroscience questions. In real-time closed-loop neuroscience experiments, many practical issues arise, such as trial-by-trial variability, and spike sorting noise or multi-unit activity. In this paper, we propose a new framework for change-point detection based on ensembles of independent detectors in the context of BMI application for detecting acute pain signals. Motivated from ensemble learning, our proposed “ensembles of change-point detectors” (ECPDs) integrate multiple decisions from independent detectors, which may be derived based on data recorded from different trials, data recorded from different brain regions, data of different modalities, or models derived from different learning methods. By integrating multiple sources of information, the ECPDs aim to improve detection accuracy (in terms of true positive and true negative rates) and achieve an optimal trade-off of sensitivity and specificity. We validate our method using computer simulations and experimental recordings from freely behaving rats. Our results have shown superior and robust performance of ECPDS in detecting the onset of acute pain signals based on neuronal population spike activity (or combined with local field potentials) recorded from single or multiple brain regions.
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References
Aminikhanghahi, S., & Cook, D.J. (2017). A survey of methods for time series change point detection. Knowledge Information Systems, 51(2), 339–367.
Bushnell, M.C., Ceko, M., Low, L.A. (2013). Cognitive and emotional control of pain and its disruption in chronic pain. Nature Review Neuroscience, 14, 502–511.
Buzsaki, G., Anastassiou, C.A., Koch, C. (2012). The origin of extracellular fields and currents—EEG, ECoG, LFP, and spikes. Nature Reviews Neuroscience, 13, 407–420.
Chen, Z. (Ed.). (2015). Advanced State Space Methods in Neural and Clinical Data. Cambridge: Cambridge University Press.
Chen, Z., & Wang, J. (2016). Statistical analysis of neuronal population codes for encoding acute pain. In Proceedings of IEEE ICASSP (pp. 829–833).
Chen, Z., Zhang, Q., Tong, A.P.S., Manders, T.R., Wang, J. (2017a). Deciphering neuronal population codes for acute thermal pain. Journal of Neural Engineering, 14(3), 036023.
Chen, Z., Hu, S., Zhang, Q., Wang, J. (2017b). Quickest detection for abrupt changes in neuronal ensemble spiking activity using model-based and model-free approaches. In Proceedings of 8th International IEEE/EMBS Conference on Neural Engineering (NER’17) (pp. 481–484).
Cheppudira, B.P. (2006). Characterization of hind paw licking and lifting to noxious radiant heat in the rat with and without chronic inflammation. Journal of Neuroscience Methods, 155, 122–125.
Copits, B.A., Pullen, M.Y., Gereau R.W. IV. (2016). Spotlight on pain: optogenetic approaches for interrogating somatosensory circuits. Pain, 157, 2424–2433.
Daou, I., Tuttle, A.H., Longo, G., Wieskopf, J.S., Bonin, R.P., Ase, A.R., Wood, J.N., De Koninck, Y., Ribeiro-da Silva, A., Mogil, J.S., Sgula, P. (2013). Remote optogenetic activation and sensitization of pain pathways in freely moving mice. The Journal of Neuroscience, 33, 18631–18640.
Deuis, J.R., Dvorakova, L.S., Vetter, I. (2017). Methods used to evaluate pain behaviors in rodents. Frontiers in Molecular Neuroscience, 10, 284.
Dietterich, T.G., & Roli, F. (2000). Ensemble methods in machine learning. In Gayar, N.E., & Kittler, J. (Eds.) Multiple Classifier Systems: Springer.
Fraser, G.W., Chase, S.M., Whitford, A., Schwartz, A.B. (2009). Control of a brain-computer interface without spike sorting. Journal of Neural Engineering, 6, 055004.
Goodman, I.N., & Johnson, D.H. (2008). Information theoretic bounds on neural prosthesis effectiveness: The importance of spike sorting. In Proceedings of ICASSP’08 (pp. 5204–5207).
Gross, J., Schnitzler, A., Timmermann, L., Ploner, M. (2007). Gamma oscillations in human primary somatosensory cortex reflect pain perception. PLoS Biology, 5, e133.
Gu, L., Uhelski, M.L., Anand, S., Romero-Ortega, M., Kim, Y.T., Fuchs, P.N., Mohanty, S.K. (2015). Pain inhibition by optogenetic activation of specific anterior cingulate cortical neurons. PLoS ONE, 10, e0117746.
Harris-Bozer, A.L., & Peng, Y.B. (2016). Inflammatory pain by carrageenan recruits low-frequency local field potential changes in the anterior cingulate cortex. Neuroscience Letters, 632, 8–14.
Hu, S., Zhang, Q., Wang, J., Chen, Z. (2017). A real-time rodent neural interface for deciphering acute pain signals from neuronal ensemble spike activity. In Proceedings of 51st Asilomar Conference of Signals, Systems, and Computers (pp. 93–97).
Hu, S., Zhang, Q., Wang, J., Chen, Z. (2018). Real-time particle filtering and smoothing algorithms for detecting abrupt changes in neural ensemble spike activity. Journal of Neurophysiology, 149(4), 1394–1410.
Iyer, S.M., Vesuna, S., Ramakrishnan, C., Huynh, K., Young, S., Berndt, A., Lee, S.Y., Gorini, C.J., Deisseroth, K., Delp, S.L. (2016). Optogenetic and chemogenetic strategies for sustained inhibition of pain. Scientific Reports, 6, 30570.
Jaffe, A., Nadler, B., Kluger, Y. (2015). Estimating the accuracies of multiple classifiers without labeled data. In AISTAT’15.
Kittler, J., Hatef, M., Duin, R.P.W., Matas, J. (1998). On combining classifiers. IEEE Transactions of the Pattern Analysis of Machine Intelligence, 20(3), 226–239.
Kopepcke, L., Ashida, G., Kretzberg, J. (2016). Single and multiple change point detection in spike trains: comparison of different CUSUM, methods. Frontiers in Systems Neuroscience, 10, 51.
Kuncheva, L.I. (2004). Combining pattern classifiers. Wiley: Methods and Algorithms.
Kuo, C.C., & Yen, C.T. (2005). Comparison of anterior cingulate and primary somatosensory neuronal responses to noxious laser-heat stimuli in conscious, behaving rats. Journal of Neurophysiology, 94, 1825–1836.
Lee, M., Manders, T.R., Eberle, S.E., Su, C., D’amour, J., Yang, R., Lin, H.Y., Deisseroth, K., Froemke, R.C., Wang, J. (2015). Activation of corticostriatal circuitry relieves chronic neuropathic pain. Journal of Neuroscience, 35(13), 5247–5259.
Liu, Y., & Yao, X. (1999). Ensemble learning via negative correlation. Neural Networks, 12(10), 1399–1404.
Macke, J.H., Buesing, L., Sahani, M. (2015). Estimating state and parameters in state space models of spike trains. In Chen, Z. (Ed.) Advanced State Space Methods in Neural and Clinical Data. Cambridge: Cambridge University Press.
Mallat, S. (2008). A Wavelet Tour of Signal Processing: the Sparse Way, 3rd edn. Cambridge: Academic Press.
Parisi, F., Strino, F., Nadler, B., Kluger, Y. (2014). Ranking and combining multiple predictors without labeled data. Proceedings of the National Academy of Science USA, 111(4), 1253–1258.
Peng, W.W., Xia, X.L., Yi, M., Huang, G., Zhang, Z., Iannetti, G., Hu, L. (2017). Brain oscillations reflecting pain-related behavior in freely-moving rats. Pain, 159(1), 106–118.
Perl, E.R. (2007). Ideas about pain, a historical view. Nature Reviews Neuroscience, 8, 71–80.
Pillow, J.W., Ahmadian, Y., Paninski, L. (2011). Model-based decoding, information estimation, and change-point detection techniques for multineuron spike trains. Neural Computation, 23(1), 1–45.
Raykar, V.C., Shipeng, Y., Zhao, L.H., Valdez, G.H., Florin, C., Bogoni, L., Moy, L. (2010). Learning with crowds. Journal of Machine Learning Research, 11, 1297–1322.
Scholkopf, B., & Smola, A.J. (2001). Learning with kernels: Support vector machines regularization, Optimization, and Beyond. Cambridge: MIT Press.
Taesler, P., & Rose, M. (2016). Prestimulus theta oscillations and connectivity modulate pain perception. Journal of Neuroscience, 36, 5026–5033.
Urien, L., Xiao, Z., Dale, J., Bauer, E.P., Chen, Z., Wang, J. (2018). Rate and temporal coding mechanisms in the anterior cingulate cortex for pain anticipation. Scientific Reports, 8, 8298.
Vierck, C.J., Whitsel, B.L., Favorov, O.V., Brown, A.W., Tommerdahl, M. (2013). Role of primary somatosensory cortex in the coding of pains. Pain, 154, 334–344.
Vogt, B.A. (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews Neuroscience, 6(7), 533–544.
Xie, Y., Huang, J., Willett, R. (2013). Change-point detection for high-dimensional time series with missing data. IEEE Journal of Selected Topics in Signal Processing, 7(1), 12–27.
Xu, J., & Brennan, T.J. (2011). The pathophysiology of acute pain: animal models. Current Opinion in Anaesthesiology, 24(5), 508–514.
Zhang, Y., Wang, N., Wang, J.-Y., Chang, J.-Y., Woodward, D.J., Luo, F. (2011). Ensemble encoding of nociceptive stimulus intensity in the rat medial and lateral pain systems. Molecular Pain, 7, 64.
Zhang, Q., Manders, T., Tong, A.P.S., Yang, R., Garg, A., Martinez, E., Zhou, H., Dale, J., Goyal, A., Urien, L., Yang, G., Chen, Z., Wang, J. (2017). Chronic pain induces generalized enhancement of aversion. eLife, 6, e25302.
Zhang, Q., Xiao, Z., Hu, S., Kulkarni, P., Martinez, E., Tong, A., Garg, A., Zhou, H., Chen, Z., Wang, J. (2018). Local field potential decoding of the onset and intensity of acute thermal pain in rats. Scientific Reports, 8, 8299.
Acknowledgements
The authors thank Eric J. Robinson for English proofreading. The work was supported by the NSF-CRCNS grant IIS-130764 (Z.C.), NSF-NCS grant #1835000 (Z.C., J.W.), NIH grants R01-NS100016 (Z.C., J.W.), R01-MH118928 (Z.C.) and R01-GM115384 (J.W.), as well as the China’s Natural Science Foundation #31627802 and Fundamental Research Funds for the Central Universities (Y.C.).
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Xiao, Z., Hu, S., Zhang, Q. et al. Ensembles of change-point detectors: implications for real-time BMI applications. J Comput Neurosci 46, 107–124 (2019). https://doi.org/10.1007/s10827-018-0694-8
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DOI: https://doi.org/10.1007/s10827-018-0694-8