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01-11-2012 | Research Article

Electrocorticographic (ECoG) correlates of human arm movements

Authors: Nicholas R. Anderson, Tim Blakely, Gerwin Schalk, Eric C. Leuthardt, Daniel W. Moran

Published in: Experimental Brain Research | Issue 1/2012

Abstract

Invasive and non-invasive brain–computer interface (BCI) studies have long focused on the motor cortex for kinematic control of artificial devices. Most of these studies have used single-neuron recordings or electroencephalography (EEG). Electrocorticography (ECoG) is a relatively new recording modality in BCI research that has primarily been built on successes in EEG recordings. We built on prior experiments related to single-neuron recording and quantitatively compare the extent to which different brain regions reflect kinematic tuning parameters of hand speed, direction, and velocity in both a reaching and tracing task in humans. Hand and arm movement experiments using ECoG have shown positive results before, but the tasks were not designed to tease out which kinematics are encoded. In non-human primates, the relationships among these kinematics have been more carefully documented, and we sought to begin elucidating that relationship in humans using ECoG. The largest modulation in ECoG activity for direction, speed, and velocity representation was found in the primary motor cortex. We also found consistent cosine tuning across both tasks, to hand direction and velocity in the high gamma band (70–160 Hz). Thus, the results of this study clarify the neural substrates involved in encoding aspects of motor preparation and execution and confirm the important role of the motor cortex in BCI applications.

Anderson NR, Wisneski K, Eisenman L, Moran DW, Leuthardt EC, Krusienski DJ (2009) An offline evaluation of the autoregressive spectrum for electrocorticography. IEEE Trans Biomed Eng 56(3):913–916. doi:10.1109/TBME.2009.2009767 PubMedCrossRef

Baker SN, Philbin N, Spinks R, Pinches EM, Wolpert DM, MacManus DG, Pauluis Q, Lemon RN (1999) Multiple single unit recording in the cortex of monkeys using independently moveable microelectrodes. J Neurosci Methods 94(1):5–17PubMedCrossRef

Blake AJ, Rodgers FC, Bassuener A, Hippensteel JA, Pearce TM, Pearce TR, Zarnowska ED, Pearce RA, Williams JC (2010) A microfluidic brain slice perfusion chamber for multisite recording using penetrating electrodes. J Neurosci Methods. doi:10.1016/j.jneumeth.2010.02.017 PubMed

Bullara LA, Agnew WF, Yuen TG, Jacques S, Pudenz RH (1979) Evaluation of electrode array material for neural prostheses. Neurosurgery 5(6):681–686PubMedCrossRef

Caminiti R, Johnson PB, Urbano A (1990) Making arm movements within different parts of space: dynamic aspects in the primate motor cortex. J Neurosci 10(7):2039–2058PubMed

Chao ZC, Nagasaka Y, Fujii N (2010) Long-term asynchronous decoding of arm motion using electrocorticographic signals in monkeys. Front Neuroeng 3:3. doi:10.3389/fneng.2010.00003 PubMed

Crone NE, Miglioretti DL, Gordon B, Lesser RP (1998) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121(Pt 12):2301–2315PubMedCrossRef

Dobelle WH, Stensaas SS, Mladejovsky MG, Smith JB (1973) A prosthesis for the deaf based on cortical stimulation. Ann Otol Rhinol Laryngol 82(4):445–463PubMed

Ganguly K, Carmena JM (2009) Emergence of a stable cortical map for neuroprosthetic control. PLoS Biol 7(7):e1000153. doi:10.1371/journal.pbio.1000153 PubMedCrossRef

Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT (1982) On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 2(11):1527–1537PubMed

Georgopoulos A, Lurito J, Petrides M, Schwartz A, Massey J (1989) Mental rotation of the neuronal population vector. Science 243:234–236PubMedCrossRef

Heldman DA, Wang W, Chan SS, Moran DW (2006) Local field potential spectral tuning in motor cortex during reaching. IEEE Trans Neural Syst Rehabil Eng 14(2):180–183PubMedCrossRef

Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M, Caplan AH, Branner A, Chen D, Penn RD, Donoghue JPD-n (2006) Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442(7099):164–171PubMedCrossRef

Klobassa DS, Vaughan TM, Brunner P, Schwartz NE, Wolpaw JR, Neuper C, Sellers EW (2009) Toward a high-throughput auditory P300-based brain-computer interface. Clin Neurophysiol 120(7):1252–1261. doi:10.1016/j.clinph.2009.04.019 PubMedCrossRef

Kubanek J, Miller KJ, Ojemann JG, Wolpaw JR, Schalk G (2009) Decoding flexion of individual fingers using electrocorticographic signals in humans. J Neural Eng 6(6):066001. doi:10.1088/1741-2560/6/6/066001 PubMedCrossRef

Kubler A, Nijboer F, Mellinger J, Vaughan TM, Pawelzik H, Schalk G, McFarland DJ, Birbaumer N, Wolpaw JR (2005) Patients with ALS can use sensorimotor rhythms to operate a brain-computer interface. Neurology 64(10):1775–1777. doi:10.1212/01.WNL.0000158616.43002.6D PubMedCrossRef

Leuthardt EC, Schalk G, Wolpaw JR, Ojemann JG, Moran DW (2004) A brain-computer interface using electrocorticographic signals in humans. J Neural Eng 1(2):63–71PubMedCrossRef

Leuthardt EC, Miller KJ, Schalk G, Rao RPN, Ojemann JG (2006a) Electrocorticography-based brain computer interface—The Seattle Experience. IEEE Trans Neural Syst Rehabil Eng 14(2):194–198

Leuthardt EC, Schalk G, Moran D, Ojemann JG (2006b) The emerging world of motor neuroprosthetics. A neurosurgical perspective. Neurosurgery 59(1):1–14PubMedCrossRef

Liu X, McCreery DB, Carter RR, Bullara LA, Yuen TG, Agnew WF (1999) Stability of the interface between neural tissue and chronically implanted intracortical microelectrodes. IEEE Trans Rehabil Eng 7(3):315–326PubMedCrossRef

Miller KJ, Leuthardt EC, Schalk G, Rao RP, Anderson NR, Moran DW, Miller JW, Ojemann JG (2007) Spectral changes in cortical surface potentials during motor movement. J Neurosci 27(9):2424–2432. doi:10.1523/JNEUROSCI.3886-06.2007 PubMedCrossRef

Miller KJ, Shenoy P, den Nijs M, Sorensen LB, Rao RN, Ojemann JG (2008) Beyond the gamma band: the role of high-frequency features in movement classification. IEEE Trans Biomed Eng 55(5):1634–1637. doi:10.1109/TBME.2008.918569 PubMedCrossRef

Moran DW, Schwartz AB (1999a) Motor cortical representation of speed and direction during reaching. J Neurophysiol 82(5):2676–2692PubMed

Moran DW, Schwartz AB (1999b) Motor cortical activity during drawing movements: population representation during spiral tracing. J Neurophysiol 82(5):2693–2704PubMed

Nijboer F, Sellers EW, Mellinger J, Jordan MA, Matuz T, Furdea A, Halder S, Mochty U, Krusienski DJ, Vaughan TM, Wolpaw JR, Birbaumer N, Kubler A (2008) A P300-based brain-computer interface for people with amyotrophic lateral sclerosis. Clin Neurophysiol 119(8):1909–1916. doi:10.1016/j.clinph.2008.03.034 PubMedCrossRef

Nunez PL, Srinivasan R (2006) Electric fields of the brain: The neurophysics of EEG, 2nd edn. Oxford University Press, OxfordCrossRef

Pistohl T, Ball T, Schulze-Bonhage A, Aertsen A, Mehring C (2008) Prediction of arm movement trajectories from ECoG-recordings in humans. J Neurosci Methods 167(1):105–114. doi:10.1016/j.jneumeth.2007.10.001 PubMedCrossRef

Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical Recipes in C

Retterer ST, Smith KL, Bjornsson CS, Turner JN, Isaacson MS, Shain W (2008) Constant pressure fluid infusion into rat neocortex from implantable microfluidic devices. J Neural Eng 5(4):385–391. doi:10.1088/1741-2560/5/4/003 PubMedCrossRef

Sanchez JC, Gunduz A, Carney PR, Principe JC (2008) Extraction and localization of mesoscopic motor control signals for human ECoG neuroprosthetics. J Neurosci Methods 167(1):63–81. doi:10.1016/j.jneumeth.2007.04.019 PubMedCrossRef

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(6):1034–1043PubMedCrossRef

Schalk G, Kubánek J, Miller KJ, Anderson NR, Leuthardt EC, Ojemann JG, Limbrick D, Moran D, Gerhardt LA, Wolpaw JR (2007a) Decoding two-dimensional movement trajectories using electrocorticographic signals in humans. J Neural Eng 4(3):264. doi: 10.1088/1741-2560/4/3/012

Schalk G, Kubanek J, Miller KJ, Anderson NR, Leuthardt EC, Ojemann JG, Limbrick D, Moran D, Gerhardt LA, Wolpaw JR (2007b) Decoding two-dimensional movement trajectories using electrocorticographic signals in humans. J Neural Eng 4(3):264–275. doi:10.1088/1741-2560/4/3/012 PubMedCrossRef

Schalk G, Miller KJ, Anderson NR, Wilson JA, Smyth MD, Ojemann JG, Moran DW, Wolpaw JR, Leuthardt EC (2008) Two-dimensional movement control using electrocorticographic signals in humans. J Neural Eng 5(1):75–84. doi:10.1088/1741-2560/5/1/008 PubMedCrossRef

Schwartz AB, Moran DW (1999) Motor cortical activity during drawing movements: population representation during lemniscate tracing. J Neurophysiol 82(5):2705–2718PubMed

Schwartz AB, Kettner RE, Georgopoulos AP (1988) Primate motor cortex and free arm movements to visual targets in three-dimensional space. I. Relations between single cell discharge and direction of movement. J Neurosci 8(8):2913–2927PubMed

Schwartz AB, Cui XT, Weber DJ, Moran DW (2006) Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 52(1):205–220. doi:10.1016/j.neuron.2006.09.019 PubMedCrossRef

Serruya MD, Hatsopoulos NG, Paninski L, Fellows MR, Donoghue JP (2002) Instant neural control of a movement signal. Nature 416(6877):141–142PubMedCrossRef

Taylor DM, Tillery SI, Schwartz AB (2002) Direct cortical control of 3D neuroprosthetic devices. Science 296(5574):1829–1832PubMedCrossRef

Velliste M, Pere S, Spalding MC, Whitford AS, Schwartz AB (2008) Cortical control of a prosthetic arm for self-feeding. Nature 453:1098–1101. doi: 10.1038/nature06996

Wang W, Chan SS, Heldman DA, Moran DW (2007) Motor cortical representation of position and velocity during reaching. J Neurophysiol 97(6):4258–4270. doi:10.1152/jn.01180.2006 PubMedCrossRef

Wang W, Chan SS, Heldman DA, Moran DW (2010) Motor cortical representation of hand translation and rotation during reaching. J Neurosci 30(3):958–962. doi:10.1523/JNEUROSCI.3742-09.2010 PubMedCrossRef

Wisneski KJ, Anderson N, Schalk G, Smyth M, Moran D, Leuthardt EC (2008) Unique cortical physiology associated with ipsilateral hand movements and neuroprosthetic implications. Stroke 39(12):3351–3359. doi:10.1161/strokeaha.108.518175 PubMedCrossRef

Wolpaw JR, Birbaumer N (2005) Brain-computer interfaces for communication and control. Textbook of neural repair and rehabilitation. Cambridge University Press, Cambridge

Wolpaw JR, Birbaumer N, McFarland DJ, Pfurtscheller G, Vaughan TM (2002) Brain-computer interfaces for communication and control. Clin Neurophysiol 113(6):767–791PubMedCrossRef

Title: Electrocorticographic (ECoG) correlates of human arm movements
Authors: Nicholas R. Anderson
Tim Blakely
Gerwin Schalk
Eric C. Leuthardt
Daniel W. Moran
Publication date: 01-11-2012
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 1/2012
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-012-3226-1

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Electrocorticographic (ECoG) correlates of human arm movements

Abstract

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