Predominance of Movement Speed Over Direction in Neuronal Population Signals of Motor Cortex: Intracranial EEG Data and A Simple Explanatory Model
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
26984895
PubMed Central
PMC4869816
DOI
10.1093/cercor/bhw033
PII: bhw033
Knihovny.cz E-zdroje
- Klíčová slova
- ECoG, brain–machine interface, population signals, tuning, velocity,
- MeSH
- biomechanika MeSH
- dospělí MeSH
- elektrokortikografie MeSH
- lidé středního věku MeSH
- lidé MeSH
- mladiství MeSH
- mladý dospělý MeSH
- modely neurologické MeSH
- motorické korové centrum fyziologie MeSH
- neurony fyziologie MeSH
- neuropsychologické testy MeSH
- paže fyziologie MeSH
- pohybová aktivita fyziologie MeSH
- Check Tag
- dospělí MeSH
- lidé středního věku MeSH
- lidé MeSH
- mladiství MeSH
- mladý dospělý MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
How neuronal activity of motor cortex is related to movement is a central topic in motor neuroscience. Motor-cortical single neurons are more closely related to hand movement velocity than speed, that is, the magnitude of the (directional) velocity vector. Recently, there is also increasing interest in the representation of movement parameters in neuronal population activity, such as reflected in the intracranial EEG (iEEG). We show that in iEEG, contrasting to what has been previously found on the single neuron level, speed predominates over velocity. The predominant speed representation was present in nearly all iEEG signal features, up to the 600-1000 Hz range. Using a model of motor-cortical signals arising from neuronal populations with realistic single neuron tuning properties, we show how this reversal can be understood as a consequence of increasing population size. Our findings demonstrate that the information profile in large population signals may systematically differ from the single neuron level, a principle that may be helpful in the interpretation of neuronal population signals in general, including, for example, EEG and functional magnetic resonance imaging. Taking advantage of the robust speed population signal may help in developing brain-machine interfaces exploiting population signals.
Zobrazit více v PubMed
Abramowitz M, Stegun IA. 1970. Handbook of mathematical functions with formulas, graphs, and mathematical tables. Dover, Ninth printing. Table 25.2.
Amirikian B, Georgopoulos AP. 2003. Modular organization of directionally tuned cells in the motor cortex: is there a short-range order? Proc Natl Acad Sci USA. 100:12474–12479. PubMed PMC
Anderson NR, Blakely T, Schalk G, Leuthardt EC, Moran DW. 2012. Electrocorticographic (ECoG) correlates of human arm movements. Exp Brain Res. 223:1–10. PubMed
Ashe J, Georgopoulos AP. 1994. Movement parameters and neural activity in motor cortex and area 5. Cereb Cortex. 4:590–600. PubMed
Ball T, Schulze-Bonhage A, Aertsen A, Mehring C. 2009. Differential representation of arm movement direction in relation to cortical anatomy and function. J Neural Eng. 6:016006. PubMed
Bansal AK, Vargas-Irwin CE, Truccolo W, Donoghue JP. 2011. Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices. J Neurophysiol. 105:1603–1619. PubMed PMC
Bédard C, Kröger H, Destexhe A. 2006. Does the 1/f frequency scaling of brain signals reflect self-organized critical states? Phys Rev Lett. 97:118102.1. PubMed
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. JRSSB. 57:289–300.
Ben-Shaul Y, Stark E, Asher I, Drori R, Nadasdy Z, Abeles M. 2003. Dynamical organization of directional tuning in the primate premotor and primary motor cortex. J Neurophysiol. 89:1136–1142. PubMed
Bourguignon M, De Tiège X, Op de Beeck M, Pirotte B, Van Bogaert P, Goldman S, Hari R, Jousmäki V. 2011. Functional motor-cortex mapping using corticokinematic coherence. Neuroimage. 55:1475–1479. PubMed
Bradberry TJ, Gentili RJ, Contreras-Vidal JL. 2010. Reconstructing three-dimensional hand movements from noninvasive electroencephalographic signals. J Neurosci. 30:3432–3437. PubMed PMC
Carmena JM, Lebedev MA, Crist RE, O'Doherty JE, Santucci DM, Dimitrov DF, Patil PG, Henriquez CS, Nicolelis MA. 2003. Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol. 1:E42. PubMed PMC
Chen R, Yaseen Z, Cohen LG, Hallett M. 1998. Time course of corticospinal excitability in reaction time and self-paced movements. Ann Neurol. 44:317–325. PubMed
Churchland MM, Shenoy KV. 2007. Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. J Neurophysiol. 97:4235–4257. 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. 121:2301–2315. PubMed
Crone NE, Sinai A, Korzeniewska A. 2006. High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res. 159:275–295. PubMed
Curio G, Mackert BM, Burghoff M, Koetitz R, Abraham-Fuchs K, Härer W. 1994. Localization of evoked neuromagnetic 600 Hz activity in the cerebral somatosensory system. Electroencephalogr Clin Neurophysiol. 91:483–487. PubMed
Dümpelmann M, Ball T, Schulze-Bonhage A. 2012. sLORETA allows reliable distributed source reconstruction based on subdural strip and grid recordings. Hum Brain Mapp. 33:1172–1188. PubMed PMC
Eccles JC. 1951. Interpretation of action potentials evoked in the cerebral cortex. Electroencephalogr Clin Neurophysiol. 3:449–464. PubMed
Edwards E, Soltani M, Deouell LY, Berger MS, Knight RT. 2005. High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. J Neurophysiol. 94:4269–4280. PubMed
Edwards E, Soltani M, Kim W, Dalal SS, Nagarajan SS, Berger MS, Knight RT. 2009. Comparison of time-frequency responses and the event-related potential to auditory speech stimuli in human cortex. J Neurophysiol. 102:377–386. PubMed PMC
Einevoll GT, Kayser C, Logothetis NK, Panzeri S. 2013. Modelling and analysis of local field potentials for studying the function of cortical circuits. Nat Rev Neurosci. 14:770–785. PubMed
Evarts EV. 1968. Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol. 31:14–27. PubMed
Faes L, Pinna GD, Porta A, Maestri R, Nollo GD. 2004. Surrogate data analysis for assessing the significance of the coherence function. IEEE Trans Biomed Eng. 51:1156–1166. PubMed
Fedele T, Scheer HJ, Burghoff M, Curio G, Körber R. 2015. Ultra-low-noise EEG/MEG systems enable bimodal non-invasive detection of spike-like human somatosensory evoked responses at 1 kHz. Physiol Meas. 36:357–368. PubMed
Fedele T, Scheer HJ, Waterstraat G, Telenczuk B, Burghoff M, Curio G. 2012. Towards non-invasive multi-unit spike recordings: mapping 1kHz EEG signals over human somatosensory cortex. Clin Neurophysiol. 123:2370–2376. PubMed
Fetz EE. 1992. Are movement parameters recognizably coded in the activity of single neurons? Behav Brain Sci. 15:679–690.
Fischer J, Milekovic T, Schneider G, Mehring C. 2014. Low-latency multi-threaded processing of neuronal signals for brain-computer interfaces. Front Neuroeng. 7:1. PubMed PMC
Flament D, Hore J. 1988. Relations of motor cortex neural discharge to kinematics of passive and active elbow movements in the monkey. J Neurophysiol. 60:1268–1284. PubMed
Fu QG, Flament D, Coltz JD, Ebner TJ. 1995. Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. J Neurophysiol. 73:836–854. PubMed
Ganguly K, Carmena JM. 2009. Emergence of a stable cortical map for neuroprosthetic control. PLoS Biol. 7:e1000153. PubMed PMC
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. 2:1527–1537. PubMed PMC
Georgopoulos AP, Langheim FJ, Leuthold AC, Merkle AN. 2005. Magnetoencephalographic signals predict movement trajectory in space. Exp Brain Res. 167:132–135. PubMed
Georgopoulos AP, Merchant H, Naselaris T, Amirikian B. 2007. Mapping of the preferred direction in the motor cortex. Proc Natl Acad Sci USA. 104:11068–11072. PubMed PMC
Georgopoulos AP, Schwartz AB, Kettner RE. 1986. Neuronal population coding of movement direction. Science. 233:1416–1419. PubMed
Golub MD, Yu BM, Schwartz AB, Chase SM. 2014. Motor cortical control of movement speed with implications for brain-machine interface control. J Neurophysiol. 112:411–429. PubMed PMC
Graziano MSA. 2011. New insights into motor cortex. Neuron. 71:387–388. PubMed
Hammer J, Fischer J, Ruescher J, Schulze-Bonhage A, Aertsen A, Ball T. 2013. The role of ECoG magnitude and phase in decoding position, velocity, and acceleration during continuous motor behavior. Front Neurosci. 7:200. PubMed PMC
Jerbi K, Lachaux JP, N'Diaye K, Pantazis D, Leahy RM, Garnero L, Baillet S. 2007. Coherent neural representation of hand speed in humans revealed by MEG imaging. Proc Natl Acad Sci USA. 104:7676–7681. PubMed PMC
Katzner S, Nauhaus I, Benucci A, Bonin V, Ringach DL, Carandini M. 2009. Local origin of field potentials in visual cortex. Neuron. 61:35–41. PubMed PMC
Kettner RE, Schwartz AB, Georgopoulos AP. 1988. Primate motor cortex and free arm movements to visual targets in three-dimensional space. III. Positional gradients and population coding of movement direction from various movement origins. J Neurosci. 8:2938–2947. PubMed PMC
Khinchin A. 1934. Korrelationstheorie der stationären stochastischen Prozesse. Mathematische Annalen. 109:604–615.
Kim SP, Simeral JD, Hochberg LR, Donoghue JP, Black MJ. 2008. Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia. J Neural Eng. 5:455–476. PubMed PMC
Lacquaniti F, Terzuolo C, Viviani P. 1983. The law relating the kinematic and figural aspects of drawing movements. Acta Psychol (Amst). 54:115–130. PubMed
Lebedev MA, Nicolelis MA. 2006. Brain-machine interfaces: past, present and future. Trends Neurosci. 29:536–546. PubMed
Łęski S, Lindén H, Tetzlaff T, Pettersen KH, Einevoll GT. 2013. Frequency dependence of signal power and spatial reach of the local field potential. PLoS Comput Biol. 9:e1003137. PubMed PMC
Lindén H, Tetzlaff T, Potjans TC, Pettersen KH, Grün S, Diesmann M, Einevoll GT. 2011. Modeling the spatial reach of the LFP. Neuron. 72:859–872. PubMed
Manning JR, Jacobs J, Fried I, Kahana MJ. 2009. Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans. J Neurosci. 29:13613–13620. PubMed PMC
Mehring C, Rickert J, Vaadia E, Cardoso de Oliveira S, Aertsen A, Rotter S. 2003. Inference of hand movements from local field potentials in monkey motor cortex. Nat Neurosci. 6:1253–1254. PubMed
Milekovic T, Fischer J, Pistohl T, Ruescher J, Schulze-Bonhage A, Aertsen A, Rickert J, Ball T, Mehring C. 2012. An online brain-machine interface using decoding of movement direction from the human electrocorticogram. J Neural Eng. 9:046003. PubMed
Miller KJ, Hermes D, Honey CJ, Hebb AO, Ramsey NF, Knight RT, Ojemann JG, Fetz EE. 2012. Human motor cortical activity is selectively phase-entrained on underlying rhythms. PLoS Comput Biol. 8:e1002655. PubMed PMC
Miller KJ, Honey CJ, Hermes D, Rao RP, denNijs M, Ojemann JG. 2014. Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations. Neuroimage. 85:711–720. PubMed PMC
Miller KJ, Leuthardt EC, Schalk G, Rao RPN, Anderson NR, Moran DW, Miller JW, Ojemann JG. 2007. Spectral changes in cortical surface potentials during motor movement. J Neurosci. 27:2424–2432. PubMed PMC
Miller KJ, Sorensen LB, Ojemann JG, den Nijs M. 2009. Power-law scaling in the brain surface electric potential. PLoS Comput Biol. 5:e1000609. PubMed PMC
Mitzdorf U. 1985. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev. 65:37–100. PubMed
Mollazadeh M, Aggarwal V, Thakor NV, Law AJ, Davidson A, Schieber MH. 2009. Coherency between spike and LFP activity in M1 during hand movements. Neural Eng. 2009. NER ‘09. 4th International IEEE/EMBS Conference on, pp. 506–509.
Moran D. 2010. Evolution of brain–computer interface: action potentials, local field potentials and electrocorticograms. Curr Opin Neurobiol. 20:741–745. PubMed PMC
Moran DW, Schwartz AB. 1999. Motor cortical representation of speed and direction during reaching. J Neurophysiol. 82:2676–2692. PubMed
Mukamel R, Fried I. 2012. Human intracranial recordings and cognitive neuroscience. Annu Rev Psychol. 63:511–537. PubMed
Mussa-Ivaldi FA. 1988. Do neurons in the motor cortex encode movement direction? An alternative hypothesis. Neurosci Lett. 91:106–111. PubMed
Naselaris T, Merchant H, Amirikian B, Georgopoulos AP. 2006. Large-Scale organization of preferred directions in the motor cortex. ii. Analysis of local distributions. J Neurophysiol. 96:3237–3247. PubMed
Nunez PL, Srinivasan R. 2006. Electric fields of the brain: the neurophysics of EEG. (2nd ed.) New York: Oxford University Press.
Nunez PL, Srinivasan R. 2010. Scale and frequency chauvinism in brain dynamics: too much emphasis on γ band oscillations. Brain Struct Funct. 215:67–71. PubMed PMC
Paninski L, Fellows MR, Hatsopoulos NG, Donoghue JP. 2004. Spatiotemporal tuning of motor cortical neurons for hand position and velocity. J Neurophysiol. 91:515–532. PubMed
Perel S, Sadtler PT, Godlove JM, Ryu SI, Wang W, Batista AP, Chase SM. 2013. Direction and speed tuning of motor-cortex multi-unit activity and local field potentials during reaching movements. Conf Proc IEEE Eng Med Biol Soc. 2013:299–230. PubMed PMC
Pfurtscheller G, Lopes da Silva FH. 1999. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. 110:1842–1857. PubMed
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. 167:105–115. PubMed
Ray S, Crone NE, Niebur E, Franaszczuk PJ, Hsiao SS. 2008. Neural correlates of high-gamma oscillations (60-200 hz) in macaque local field potentials and their potential implications in electrocorticography. J Neurosci. 28:11526–11536. PubMed PMC
Ray S, Maunsell JH. 2011. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol. 9:e1000610. PubMed PMC
Rickert J, Oliveira SC, Vaadia E, Aertsen A, Rotter S, Mehring C. 2005. Encoding of movement direction in different frequency ranges of motor cortical local field potentials. J Neurosci. 28:8815–8824. PubMed PMC
Sauseng P, Klimesch W. 2008. What does phase information of oscillatory brain activity tell us about cognitive processes? Neurosci Biobehav Rev. 32:1001–1013. PubMed
Schalk G, Kubánek J, Miller KJ, Anderson NR, Leuthardt EC, Ojemann JG, Limbrick D, Moran DW, Gerhardt LA, Wolpaw JR. 2007. Decoding two-dimensional movement trajectories using electrocorticographic signals in humans. J Neural Eng. 4:264–275. PubMed
Schwartz AB. 1994. Direct cortical representation of drawing. Science. 265:540–542. PubMed
Schwartz AB, Cui XT, Weber DJ, Moran DW. 2006. Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 52:205–220. PubMed
Schwartz AB, Moran DW. 1999. Motor cortical activity during drawing movements: population representation during lemniscate tracing. J Neurophysiol. 82:2705–2718. PubMed
Sergio LE, Hamel-Paquet C, Kalaska JF. 2005. Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. J Neurophysiol. 94:2353–2378. PubMed
Stark E, Drori R, Abeles M. 2009. Motor Cortical activity related to movement kinematics exhibits local spatial organization. Cortex. 45:418–431. PubMed
Todorov E. 2000. Direct cortical control of muscle activation in voluntary arm movements: a model. Nat Neurosci. 3:391–398. PubMed
Vaadia E, Birbaumer N. 2009. Grand challenges of brain computer interfaces in the years to come. Front Neurosci. 3:151–154. PubMed PMC
Waldert S, Pistohl T, Braun C, Ball T, Aertsen A, Mehring C. 2009. A review on directional information in neural signals for brain–machine interfaces. J Physiol Paris. 103:244–254. PubMed
Waldert S, Preissl H, Demandt E, Braun C, Birbaumer N, Aertsen A, Mehring C. 2008. Hand movement direction decoded from MEG and EEG. J Neurosci. 28:1000–1008. PubMed PMC
Wander JD, Blakely T, Miller KJ, Weaver KE, Johnson LA, Olson JD, Fetz EE, Rao RP, Ojemann JG. 2013. Distributed cortical adaptation during learning of a brain-computer interface task. Proc Natl Acad Sci USA. 110:10818–10823. PubMed PMC
Wolpaw JR, McFarland DJ, Vaughan TM, Schalk G. 2003. The Wadsworth Center brain-computer interface (BCI) research and development program. IEEE Trans Neural Syst Rehab Eng. 11:204–207. PubMed
Timing of Allocentric and Egocentric Spatial Processing in Human Intracranial EEG
Mapping the Scene and Object Processing Networks by Intracranial EEG