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Chronic stability of single-channel neurophysiological correlates of gross and fine reaching movements in the rat


Autoři: David T. Bundy aff001;  David J. Guggenmos aff001;  Maxwell D. Murphy aff002;  Randolph J. Nudo aff001
Působiště autorů: Department of Rehabilitation Medicine, University of Kansas Medical Center, Kansas City, KS, United States of America aff001;  Bioengineering Graduate Program, University of Kansas, Lawrence, KS, United States of America aff002;  Landon Center on Aging, University of Kansas Medical Center, Kansas City, KS, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0219034

Souhrn

While substantial task-related neural activity has been observed during motor tasks in rodent primary motor cortex and premotor cortex, the long-term stability of these responses in healthy rats is uncertain, limiting the interpretability of longitudinal changes in the specific patterns of neural activity associated with learning or motor recovery following injury. This study examined the stability of task-related neural activity associated with execution of two distinct reaching tasks in healthy rodents. A novel automated rodent behavioral apparatus was constructed and rats were trained to perform a reaching task combining a ‘gross’ lever press and a ‘fine’ pellet retrieval. In each animal, two chronic microelectrode arrays were implanted in motor cortex spanning the caudal forelimb area (rodent primary motor cortex) and the rostral forelimb area (rodent premotor cortex). We recorded multiunit spiking and local field potential activity from 10 days to 7–10 weeks post-implantation to characterize the patterns of neural activity observed during each task component and analyzed the consistency of channel-specific task-related neural activity. Task-related changes in neural activity were observed on the majority of channels. While the task-related changes in multi-unit spiking and local field potential spectral power were consistent over several weeks, spectral power changes were more stable, despite the trade-off of decreased spatial and temporal resolution. These results show that neural activity in rodent primary and premotor cortex is associated with specific phases of reaching movements with stable patterns of task-related activity across time, establishing the relevance of the rodent for future studies designed to examine changes in task-related neural activity during recovery from focal cortical lesions.

Klíčová slova:

Action potentials – Animal performance – Medical implants – Microelectrodes – Neurophysiology – Primates – Rats – Rodents


Zdroje

1. Igarashi J, Isomura Y, Arai K, Harukuni R, Fukai T. A theta-gamma oscillation code for neuronal coordination during motor behavior. J Neurosci. 2013;33(47):18515–30. doi: 10.1523/JNEUROSCI.2126-13.2013 24259574.

2. Slutzky MW, Jordan LR, Bauman MJ, Miller LE. A new rodent behavioral paradigm for studying forelimb movement. J Neurosci Methods. 2010;192(2):228–32. Epub 2010/08/10. doi: 10.1016/j.jneumeth.2010.07.040 20691727; PubMed Central PMCID: PMC2943042.

3. Hermer-Vazquez L, Hermer-Vazquez R, Chapin JK. The reach-to-grasp-food task for rats: a rare case of modularity in animal behavior? Behav Brain Res. 2007;177(2):322–8. doi: 10.1016/j.bbr.2006.11.029 17207541; PubMed Central PMCID: PMC1885543.

4. Whishaw IQ, Pellis SM. The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component. Behav Brain Res. 1990;41(1):49–59. Epub 1990/12/07. doi: 10.1016/0166-4328(90)90053-h 2073355.

5. Chapin JK, Moxon KA, Markowitz RS, Nicolelis MA. Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nat Neurosci. 1999;2(7):664–70. doi: 10.1038/10223 10404201.

6. Gulati T, Won SJ, Ramanathan DS, Wong CC, Bodepudi A, Swanson RA, et al. Robust neuroprosthetic control from the stroke perilesional cortex. J Neurosci. 2015;35(22):8653–61. doi: 10.1523/JNEUROSCI.5007-14.2015 26041930.

7. Hyland B. Neural activity related to reaching and grasping in rostral and caudal regions of rat motor cortex. Behav Brain Res. 1998;94(2):255–69. doi: 10.1016/s0166-4328(97)00157-5 9722277.

8. Laubach M, Wessberg J, Nicolelis MA. Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature. 2000;405(6786):567–71. doi: 10.1038/35014604 10850715.

9. Nishibe M, Barbay S, Guggenmos D, Nudo RJ. Reorganization of motor cortex after controlled cortical impact in rats and implications for functional recovery. J Neurotrauma. 2010;27(12):2221–32. doi: 10.1089/neu.2010.1456 20873958; PubMed Central PMCID: PMC2996815.

10. Nishibe M, Urban ET, 3rd, Barbay S, Nudo RJ. Rehabilitative training promotes rapid motor recovery but delayed motor map reorganization in a rat cortical ischemic infarct model. Neurorehabil Neural Repair. 2015;29(5):472–82. doi: 10.1177/1545968314543499 25055836; PubMed Central PMCID: PMC4303553.

11. Slutzky MW, Jordan LR, Lindberg EW, Lindsay KE, Miller LE. Decoding the rat forelimb movement direction from epidural and intracortical field potentials. J Neural Eng. 2011;8(3):036013. doi: 10.1088/1741-2560/8/3/036013 21508491; PubMed Central PMCID: PMC3124348.

12. Neafsey EJ, Sievert C. A second forelimb motor area exists in rat frontal cortex. Brain Res. 1982;232(1):151–6. Epub 1982/01/28. doi: 10.1016/0006-8993(82)90617-5 7055691.

13. Rouiller EM, Moret V, Liang F. Comparison of the connectional properties of the two forelimb areas of the rat sensorimotor cortex: support for the presence of a premotor or supplementary motor cortical area. Somatosens Mot Res. 1993;10(3):269–89. Epub 1993/01/01. 8237215.

14. Sievert CF, Neafsey EJ. A chronic unit study of the sensory properties of neurons in the forelimb areas of rat sensorimotor cortex. Brain Res. 1986;381(1):15–23. Epub 1986/08/27. doi: 10.1016/0006-8993(86)90684-0 3530375.

15. Deffeyes JE, Touvykine B, Quessy S, Dancause N. Interactions between rostral and caudal cortical motor areas in the rat. J Neurophysiol. 2015;113(10):3893–904. doi: 10.1152/jn.00760.2014 25855697; PubMed Central PMCID: PMC4480625.

16. Whishaw IQ, Alaverdashvili M, Kolb B. The problem of relating plasticity and skilled reaching after motor cortex stroke in the rat. Behav Brain Res. 2008;192(1):124–36. doi: 10.1016/j.bbr.2007.12.026 18282620.

17. Whishaw IQ, Pellis SM, Gorny BP, Pellis VC. The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis. Behav Brain Res. 1991;42(1):77–91. doi: 10.1016/s0166-4328(05)80042-7 2029348.

18. Guggenmos DJ, Azin M, Barbay S, Mahnken JD, Dunham C, Mohseni P, et al. Restoration of function after brain damage using a neural prosthesis. Proc Natl Acad Sci U S A. 2013;110(52):21177–82. doi: 10.1073/pnas.1316885110 24324155; PubMed Central PMCID: PMC3876197.

19. Quiroga RQ, Nadasdy Z, Ben-Shaul Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 2004;16(8):1661–87. Epub 2004/07/02. doi: 10.1162/089976604774201631 15228749.

20. Chestek CA, Gilja V, Nuyujukian P, Foster JD, Fan JM, Kaufman MT, et al. Long-term stability of neural prosthetic control signals from silicon cortical arrays in rhesus macaque motor cortex. J Neural Eng. 2011;8(4):045005. Epub 2011/07/22. doi: 10.1088/1741-2560/8/4/045005 21775782; PubMed Central PMCID: PMC3644617.

21. Marple SL Jr, Carey WM. Digital spectral analysis with applications. ASA; 1989.

22. Rasch MJ, Gretton A, Murayama Y, Maass W, Logothetis NK. Inferring spike trains from local field potentials. J Neurophysiol. 2008;99(3):1461–76. doi: 10.1152/jn.00919.2007 18160425.

23. Ellens DJ, Gaidica M, Toader A, Peng S, Shue S, John T, et al. An automated rat single pellet reaching system with high-speed video capture. J Neurosci Methods. 2016;271:119–27. doi: 10.1016/j.jneumeth.2016.07.009 27450925; PubMed Central PMCID: PMC5003677.

24. Wong CC, Ramanathan DS, Gulati T, Won SJ, Ganguly K. An automated behavioral box to assess forelimb function in rats. J Neurosci Methods. 2015;246:30–7. Epub 2015/03/15. doi: 10.1016/j.jneumeth.2015.03.008 25769277; PubMed Central PMCID: PMC5472046.

25. Flint RD, Lindberg EW, Jordan LR, Miller LE, Slutzky MW. Accurate decoding of reaching movements from field potentials in the absence of spikes. J Neural Eng. 2012;9(4):046006. Epub 2012/06/27. doi: 10.1088/1741-2560/9/4/046006 22733013; PubMed Central PMCID: PMC3429374.

26. Jensen W, Rousche PJ. Encoding of self-paced, repetitive forelimb movements in rat primary motor cortex. Conf Proc IEEE Eng Med Biol Soc. 2004;6:4233–6. doi: 10.1109/IEMBS.2004.1404180 17271238.

27. Khorasani A, Heydari Beni N, Shalchyan V, Daliri MR. Continuous Force Decoding from Local Field Potentials of the Primary Motor Cortex in Freely Moving Rats. Sci Rep. 2016;6:35238. Epub 2016/10/22. doi: 10.1038/srep35238 27767063; PubMed Central PMCID: PMC5073334.

28. Saiki A, Kimura R, Samura T, Fujiwara-Tsukamoto Y, Sakai Y, Isomura Y. Different modulation of common motor information in rat primary and secondary motor cortices. PLoS One. 2014;9(6):e98662. doi: 10.1371/journal.pone.0098662 24893154; PubMed Central PMCID: PMC4043846.

29. Poddar R, Kawai R, Olveczky BP. A fully automated high-throughput training system for rodents. PLoS One. 2013;8(12):e83171. doi: 10.1371/journal.pone.0083171 24349451; PubMed Central PMCID: PMC3857823.

30. Kurata K, Tanji J. Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci. 1986;6(2):403–11. Epub 1986/02/01. 3950703.

31. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M. Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res. 1988;71(3):491–507. Epub 1988/01/01. doi: 10.1007/bf00248742 3416965.

32. Brown AR, Teskey GC. Motor cortex is functionally organized as a set of spatially distinct representations for complex movements. J Neurosci. 2014;34(41):13574–85. doi: 10.1523/JNEUROSCI.2500-14.2014 25297087.

33. Dickey AS, Suminski A, Amit Y, Hatsopoulos NG. Single-unit stability using chronically implanted multielectrode arrays. J Neurophysiol. 2009;102(2):1331–9. doi: 10.1152/jn.90920.2008 19535480; PubMed Central PMCID: PMC2724357.

34. Perge JA, Homer ML, Malik WQ, Cash S, Eskandar E, Friehs G, et al. Intra-day signal instabilities affect decoding performance in an intracortical neural interface system. J Neural Eng. 2013;10(3):036004. doi: 10.1088/1741-2560/10/3/036004 23574741; PubMed Central PMCID: PMC3693851.

35. Rokni U, Richardson AG, Bizzi E, Seung HS. Motor learning with unstable neural representations. Neuron. 2007;54(4):653–66. Epub 2007/05/25. doi: 10.1016/j.neuron.2007.04.030 17521576.

36. Chestek CA, Batista AP, Santhanam G, Yu BM, Afshar A, Cunningham JP, et al. Single-neuron stability during repeated reaching in macaque premotor cortex. J Neurosci. 2007;27(40):10742–50. Epub 2007/10/05. doi: 10.1523/JNEUROSCI.0959-07.2007 17913908; PubMed Central PMCID: PMC6672821.

37. Stevenson IH, Cherian A, London BM, Sachs NA, Lindberg E, Reimer J, et al. Statistical assessment of the stability of neural movement representations. J Neurophysiol. 2011;106(2):764–74. Epub 2011/05/27. doi: 10.1152/jn.00626.2010 21613593; PubMed Central PMCID: PMC3154833.

38. Flint RD, Scheid MR, Wright ZA, Solla SA, Slutzky MW. Long-Term Stability of Motor Cortical Activity: Implications for Brain Machine Interfaces and Optimal Feedback Control. J Neurosci. 2016;36(12):3623–32. Epub 2016/03/26. doi: 10.1523/JNEUROSCI.2339-15.2016 27013690; PubMed Central PMCID: PMC4804017.


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