Reliability of Directional Information in Unsorted Spikes and Local Field Potentials Recorded in Human Motor Cortex

Overview

Journal J Neural Eng

Specialties Biomedical Engineering
Neurology

Date 2014 Jun 13

PMID 24921388

Citations 42

Authors

Janos A Perge

Shaomin Zhang

Wasim Q Malik

Mark L Homer

Sydney Cash

Gerhard Friehs

Emad N Eskandar

John P Donoghue

Leigh R Hochberg

Affiliations

Soon will be listed here.

Abstract

Objective: Action potentials and local field potentials (LFPs) recorded in primary motor cortex contain information about the direction of movement. LFPs are assumed to be more robust to signal instabilities than action potentials, which makes LFPs, along with action potentials, a promising signal source for brain-computer interface applications. Still, relatively little research has directly compared the utility of LFPs to action potentials in decoding movement direction in human motor cortex.

Approach: We conducted intracortical multi-electrode recordings in motor cortex of two persons (T2 and [S3]) as they performed a motor imagery task. We then compared the offline decoding performance of LFPs and spiking extracted from the same data recorded across a one-year period in each participant.

Main Results: We obtained offline prediction accuracy of movement direction and endpoint velocity in multiple LFP bands, with the best performance in the highest (200-400 Hz) LFP frequency band, presumably also containing low-pass filtered action potentials. Cross-frequency correlations of preferred directions and directional modulation index showed high similarity of directional information between action potential firing rates (spiking) and high frequency LFPs (70-400 Hz), and increasing disparity with lower frequency bands (0-7, 10-40 and 50-65 Hz). Spikes predicted the direction of intended movement more accurately than any individual LFP band, however combined decoding of all LFPs was statistically indistinguishable from spike-based performance. As the quality of spiking signals (i.e. signal amplitude) and the number of significantly modulated spiking units decreased, the offline decoding performance decreased 3.6[5.65]%/month (for T2 and [S3] respectively). The decrease in the number of significantly modulated LFP signals and their decoding accuracy followed a similar trend (2.4[2.85]%/month, ANCOVA, p = 0.27[0.03]).

Significance: Field potentials provided comparable offline decoding performance to unsorted spikes. Thus, LFPs may provide useful external device control using current human intracortical recording technology. (

Clinical Trial Registration Number: NCT00912041.).

Citing Articles

Neural signal analysis in chronic stroke: advancing intracortical brain-computer interface design.

Shawki N, Napoli A, Vargas-Irwin C, Thompson C, Donoghue J, Serruya M Front Hum Neurosci. 2025; 19:1544397.

PMID: 40060267 PMC: 11885313. DOI: 10.3389/fnhum.2025.1544397.

[Ethical considerations for medical applications of implantable brain-computer interfaces].

Zhang Z, Chen Y, Zhao X, Wang F, Ding P, Zhao L Sheng Wu Yi Xue Gong Cheng Xue Za Zhi. 2024; 41(1):177-183.

PMID: 38403619 PMC: 10894729. DOI: 10.7507/1001-5515.202309083.

Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex.

Shih W, Yu H, Lee C, Chou C, Chen C, Glimcher P Nat Commun. 2023; 14(1):7821.

PMID: 38016973 PMC: 10684521. DOI: 10.1038/s41467-023-42092-x.

ROSE: A Neurocomputational Architecture for Syntax.

Murphy E ArXiv. 2023; .

PMID: 36994166 PMC: 10055479.

Chronic Stability of Local Field Potentials Using Amorphous Silicon Carbide Microelectrode Arrays Implanted in the Rat Motor Cortex.

Jeakle E, Abbott J, Usoro J, Wu Y, Haghighi P, Radhakrishna R Micromachines (Basel). 2023; 14(3).

PMID: 36985087 PMC: 10054633. DOI: 10.3390/mi14030680.

References

Wanifuchi H, Shimizu T, Maruyama T . Age-related changes in the proportion of intracranial cerebrospinal fluid space measured using volumetric computerized tomography scanning. J Neurosurg. 2002; 97(3):607-10. DOI: 10.3171/jns.2002.97.3.0607. View

Perge J, Homer M, Malik W, Cash S, Eskandar E, Friehs G . Intra-day signal instabilities affect decoding performance in an intracortical neural interface system. J Neural Eng. 2013; 10(3):036004. PMC: 3693851. DOI: 10.1088/1741-2560/10/3/036004. View

Mehring C, Rickert J, Vaadia E, Cardosa de Oliveira S, Aertsen A, Rotter S . Inference of hand movements from local field potentials in monkey motor cortex. Nat Neurosci. 2003; 6(12):1253-4. DOI: 10.1038/nn1158. View

Gold C, Henze D, Koch C, Buzsaki G . On the origin of the extracellular action potential waveform: A modeling study. J Neurophysiol. 2006; 95(5):3113-28. DOI: 10.1152/jn.00979.2005. View

Serruya M, Hatsopoulos N, Paninski L, Fellows M, Donoghue J . Instant neural control of a movement signal. Nature. 2002; 416(6877):141-2. DOI: 10.1038/416141a. View

Li Z, ODoherty J, Lebedev M, Nicolelis M . Adaptive decoding for brain-machine interfaces through Bayesian parameter updates. Neural Comput. 2011; 23(12):3162-204. PMC: 3335277. DOI: 10.1162/NECO_a_00207. View

Katzner S, Nauhaus I, Benucci A, Bonin V, Ringach D, Carandini M . Local origin of field potentials in visual cortex. Neuron. 2009; 61(1):35-41. PMC: 2730490. DOI: 10.1016/j.neuron.2008.11.016. View

Ganguly K, Carmena J . Emergence of a stable cortical map for neuroprosthetic control. PLoS Biol. 2009; 7(7):e1000153. PMC: 2702684. DOI: 10.1371/journal.pbio.1000153. View

Georgopoulos A, Merchant H, Naselaris T, Amirikian B . Mapping of the preferred direction in the motor cortex. Proc Natl Acad Sci U S A. 2007; 104(26):11068-72. PMC: 1904163. DOI: 10.1073/pnas.0611597104. View

10.

Homer M, Perge J, Black M, Harrison M, Cash S, Hochberg L . Adaptive offset correction for intracortical brain-computer interfaces. IEEE Trans Neural Syst Rehabil Eng. 2013; 22(2):239-48. PMC: 4117314. DOI: 10.1109/TNSRE.2013.2287768. View

11.

Flint R, Wright Z, Scheid M, Slutzky M . Long term, stable brain machine interface performance using local field potentials and multiunit spikes. J Neural Eng. 2013; 10(5):056005. PMC: 4023629. DOI: 10.1088/1741-2560/10/5/056005. View

12.

Zhuang J, Truccolo W, Vargas-Irwin C, Donoghue J . Reconstructing grasping motions from high-frequency local field potentials in primary motor cortex. Annu Int Conf IEEE Eng Med Biol Soc. 2010; 2010:4347-50. PMC: 3048029. DOI: 10.1109/IEMBS.2010.5626228. View

13.

Pesaran B, Pezaris J, Sahani M, Mitra P, Andersen R . Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci. 2002; 5(8):805-11. DOI: 10.1038/nn890. View

14.

Chestek C, Gilja V, Nuyujukian P, Foster J, Fan J, Kaufman M . Long-term stability of neural prosthetic control signals from silicon cortical arrays in rhesus macaque motor cortex. J Neural Eng. 2011; 8(4):045005. PMC: 3644617. DOI: 10.1088/1741-2560/8/4/045005. View

15.

Amirikian B, Georgopoulos A . Modular organization of directionally tuned cells in the motor cortex: is there a short-range order?. Proc Natl Acad Sci U S A. 2003; 100(21):12474-9. PMC: 218782. DOI: 10.1073/pnas.2037719100. View

16.

Schomburg E, Anastassiou C, Buzsaki G, Koch C . The spiking component of oscillatory extracellular potentials in the rat hippocampus. J Neurosci. 2012; 32(34):11798-811. PMC: 3459239. DOI: 10.1523/JNEUROSCI.0656-12.2012. View

17.

Harris K, Hirase H, Leinekugel X, Henze D, Buzsaki G . Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron. 2001; 32(1):141-9. DOI: 10.1016/s0896-6273(01)00447-0. View

18.

Bansal A, Truccolo W, Vargas-Irwin C, Donoghue J . Decoding 3D reach and grasp from hybrid signals in motor and premotor cortices: spikes, multiunit activity, and local field potentials. J Neurophysiol. 2011; 107(5):1337-55. PMC: 3311686. DOI: 10.1152/jn.00781.2011. View

19.

Csicsvari J, Henze D, Jamieson B, Harris K, Sirota A, Bartho P . Massively parallel recording of unit and local field potentials with silicon-based electrodes. J Neurophysiol. 2003; 90(2):1314-23. DOI: 10.1152/jn.00116.2003. View

20.

Hochberg L, Serruya M, Friehs G, Mukand J, Saleh M, Caplan A . Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature. 2006; 442(7099):164-71. DOI: 10.1038/nature04970. View