Abstract
The cerebellum, even when not directly damaged, is potentially interesting for understanding the adaptive responses to brain injury. Cerebellar electrocortical activity (ECoG) in rats was studied using spectral and fractal analysis after single and repeated unilateral injury of the parietal cortex. Local field potentials of cerebellar paravermal cortex were recorded before brain injury, in the acute phase (up to 2.5 hours) after a first injury of anesthetized rats, and then before and after second, third, and, in some cases, fourth injury. Relative gamma power (32.1–128.0 Hz) and fractal dimension of ECoGs were temporarily increased after the first injury. However, there was a permanent mild increase in gamma activity and a mild increase in the fractal dimension of cerebellar activity as a chronic change after repeated remote brain injury. There was a negative linear correlation between the normalized difference in fractal dimensions and normalized difference in gamma powers of cerebellar activity only in the case of repeated brain injury. This is the first study showing that correlation between the parameters of spectral and fractal analyses of cerebellar activity can discriminate between single and repeated brain injuries, and is, therefore, a promising approach for identifying specific pathophysiological states.
Similar content being viewed by others
References
Accardo, A., Affinito, M., Carrozzi, M., Bouquet, F., 1997. Use of the fractal dimension for the analysis of electroencephalographic time series. Biol. Cybernetics 77, 339–350.
Borgers, C., Epstein, S., Kopell, N.J., 2005. Background gamma rhythmicity and attention in cortical local circuit: A computational study. PNAS 102, 7002–7007.
Bracic, M., Stefanoska, A., 1998. Nonlinear dynamics of the blood flow studied by Lyapunov exponents. Bull. Math. Biol. 60, 417–433.
Carmichael, S.T., Chesselet, M.F., 2002. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adults. J. Neurosci. 22, 6062–6070.
Chae, J.H., Jeong, J., Peterson, B.S., Kim, J., Bahk, W.M., Jun, T.Y., Kim, S.Y., Kim, K.S., 2004. Dimensional complexity of the EEG in patients with posttraumatic stress disorder. Psychiatry Res. Neuroimaging 131, 79–89.
Chakravarty, A., 2002. Crossed cerebral-cerebellar diaschisis: MRI evaluation. Neurol. India 50, 322–325.
Choi, K.G., Cho, E.K., Chae, S.H., Kim, E.S., Kim, J.S., 1999. Spectral and bispectral EEG analysis in acute unilateral ischemic stroke patients. Neurol. Psychiatry Brain Res. 7, 9–14.
Courtemanche, R., Lamarre, Y., 2005. Local field potential oscillations in primate cerebellar cortex: Synchronization with cerebral cortex during active and passive expectancy. J. Neurophysiol. 93, 2039–2052.
Culic, M., Grbic, G., Martac, Lj., Todorovic, V., Drndarevic, N., Spasic, S., Sekulic, S., 2005a. Neocortical plasticity after repeated brain injury in rats. In: Gantchev, N. (Ed.), From Basic Motor Control to Functional Recovery IV, pp. 315–321. Marin Drinov Academic Publishing House, Sofia.
Culic, M., Martac Blanusa, L., Grbic, G., Spasic, S., Jankovic, B., Kalauzi, A., 2005b. Spectral analysis of cerebellar activity after acute brain injury in anesthetized rats. Acta Neurobiol. Exp. 65, 11–17.
Culic, M., Grbic, G., Martac, Lj., Kesic, S., Todorovic, V., Spasic, S., Sekulic, S., 2006. Cerebellar responses to traumatic brain injury in rats. In: Ruzdijic, S., Rakic, Lj. (Eds.), Neurobiological Studies—From Genes to Behaviour, pp. 167–181. Research Signpost, Trivandrum.
DeFord, M.S., Wilson, M.S., Rice, A.C., Clausen, T., Rice, L.K., Barabnova, A., Bullock, R., Hamm, R.J., 2002. Repeated mild brain injuries result in cognitive impairment in B6C3F1 mice. J. Neurotrauma 19, 427–438.
Diambra, L., Malta, C.P., Capurro, A., Fernandez, J., 2001. Nonlinear structures in electroencephalogram signals. Physica A 300, 505–520.
Eke, A., Herman, P., Kocsis, L., Kozak, L.R., 2002. Fractal characterization of complexity in temporal physiological signals. Physiol. Meas. 23, R1–R38.
Engel, A.K., Singer, W., 2001. Temporal binding and the neural correlates of sensory awareness. Trends Cogn. Sci. 5, 16–25.
Esteller, R., Vachtsevanos, G., Echauz, J., Litt, B., 1999. A comparison of fractal dimension algorithms using synthetic and experimental data. In: Proc. IEEE International Symposium on Circuits and System, Adaptive Digital Signal Processing, Orlando, Fl, III, pp. 199–202.
Eurich, C., 2003. Neural dynamics and neural coding. Ph. Thesis, University of Bremen, pp. 1–195.
Gaetz, M., 2004. The neurophysiology of brain injury. Cl. Neurophysiol. 115, 4–18.
Gianetti, S., Molinari, M., 2002. Cerebellar input to the posterior parietal cortex in the rat. Brain Res. Bull. 58, 481–489.
Goodman, J.C., Cherian, L., Bryan, R.M., Jr., Robertson, C.S., 1994. Lateral cortical impact injury in rats: pathologic effects of varying cortical compression and impact velocity. J. Neurotrauma 11, 587–597.
Gray, C.M., 1999. The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24, 31–47.
Guha, A., 2004. Head injury research: What have we learned? Ind. J. Crit. Care. Med. 8, 111–115.
Hernandez Caceres, L.J., Sibat, F.S., Hong, R., Garcia, L., Sautie, M., Namugova, V., 2004. Towards the estimation of fractal dimension of heart rate variability data. El. J. Biomed. 2, 4–15.
Higuchi, T., 1988. Approach to an irregular time series on the basis of the fractal theory. Physics D 31, 277–283.
Juhasz, C., Kamondi, A., Szirmai, I., 1997. Spectral EEG analysis following hemispheric stroke. Acta Neurol. Scand. 96, 397–400.
Jurkowlaniec, E., Tokarski, J., Trojniar, W., 2003. Effects of unilateral ibotenate lesions of the ventral tegmental area on cortical and hippocampal EEG in freely behaving rats. Acta Neurobiol. Exp. 62, 369–375.
Kalauzi, A., Spasic, S., Culic, M., Grbic, G., Martac, Lj., 2004. Correlation between fractal dimension and power spectra after unilateral cerebral injury in rat. FENS Abstr. 2, A.199.9.
Kalauzi, A., Spasic, S., Culic, M., Grbic, G., Martac, Lj., 2005. Consecutive differences as a method of signal fractal analysis. Fractals 13, 283–292.
Klonowski, W., 2002. Chaotic dynamics applied to signal complexity in phase space and in time domain. Chaos Solitons Fractals 14, 1379–1387.
Klonowski, W., Olejaczyk, E., Stepien, R., Scelenberger, W., 2003. New methods of nonlinear and symbolic dynamics in sleep EEG-signal analysis. In: Feng, D.D., Carson, E.R. (Eds.), Modelling and Control in Biomedical Systems, Proc. 5th IFAC Symposium, pp. 241–244. Elsevier, Amsterdam.
Klonowski, W., Olejaczyk, E., Stepien, R., Jalowiecki, P., Rudner, R., 2006. Monitoring the depth of anaesthesia using fractal complexity method. In: Novak, M.M. (Ed.), Complexus Mundi, Emergent Patterns in Nature, pp. 333–342. World Scientific, Singapore.
Le Van Quyen, M., 2003. Disentangling the dynamic core: a research program for a neurodynamics at he large-scale. Biol. Res. 36, 67–88.
Micheloyannis, S., Flitzanis, N., Papanikolaou, E., Bourkas, M., Terzakis, D., Arvanitis, S., Stam, C.J., 1998. Usefulness of non-linear EEG analysis. Acta Neurol. Scand. 97, 13–19.
Nitish, V., Thakor, N.T., Tong, S., 2004. Advances in quantitative electroencephalogram analysis methods. Annu. Rev. Biomed. Eng. 6, 453–495.
Orzel-Gryglewska, J., Jurkowlaniec, E., Trojnier, W., 2006. Microinjection of procaine and electrolytic lesion in the ventral tegmental area suppresses hippocampal theta rhythm in urethane-anesthetized rats. Brain Res. Bull. 68, 295–309.
Parsons, L.C., Crosby, L.J., Perlis, M., Britt, T., Jones, P., 1997. Longitudal sleep EEG power spectral analysis studies in adolescent minor head injury. J. Neurotrauma 14, 549–559.
Pradhan, N., Narayana Dutt, D., Sadasivan, P.K., Satish, M., 1995. Analysis of the chaotic characteristics of sleep EEG patterns from dominant Lyapunov exponent. In: Engineering in Medicine and Biology Society, 14th Conference of the Biomedical Engineering Society of India, 3/79–3/80.
Saini, S., DeStefano, N., Smith, S., Guidi, L., Amato, M.P., Federico, A., Matthews, P.M., 2004. Altered cerebellar functional connectivity mediates potential adaptive plasticity in patients with multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 75, 840–846.
Savi, M.A., 2005. Chaos and order in biomedical rhythms. J. Braz. Soc. Mech. Sci. Eng. 27, 157–169.
Sinai, A., Bowers, C.W., Crainiceanu, C.M., Boatman, D., Gordon, B., Lesser, R.P., Lenz, F.A., Crone, N.E., 2005. Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. Brain 128, 1556–1570.
Slemmer, J.E., Matser, E.J.T., De Zeeuw, C.I., Weber, J.T., 2002. Repeated mild injury causes cumulative damage to hippocampal cells. Brain 125, 2699–2709.
Small, S.L., Small, S.L., Hlustik, P., Noll, D.C., Genovese, C., Solodkin, A., 2002. Cerebellar hemispheric activation ipsilateral to the paretic hand correlates with functional recovery after stroke. Brain 125, 1544–1557.
Sotropoulos, D.S., Baker, S.N., 2006. Cortico-cerebellar coherence during a precision grip task in the monkey. J. Neurophysiol. 96, 1194–1206.
Spasic, S., 2007. Spectral and fractal analysis of biosignals and coloured noise. In: Proceedings of the 5th International Symposium on Intelligent Systems and Informatics, pp. 147–150. August 24–25, 2007, Subotica.
Spasic, S., Kalauzi, A., Culic, M., Grbic, G., Martac, Lj., 2005a. Fractal analysis of rat brain activity after injury. Med. Biol. Eng. Comput. 43, 345–348.
Spasic, S., Kalauzi, A., Culic, M., Grbic, G., Martac, Lj., 2005b. Estimation of parameter kmax in fractal analysis of rat brain activity. Ann. N.Y. Acad. Sci. 1048, 427–429.
Tong, T., Bezerianos, A., Paul, J., Zhu, Y., Thakor, N., 2002. Nonextensive entropy measure of EEG following brain injury from cardiac arrest. Physica A: Stat. Mech. Appl. 305, 619–628.
Tononi, G., Edelman, G.M., Sporns, O., 1998. Complexity and coherency: integrating information in the brain. Trends Cogn. Sci. 2, 474–484.
Watkins, N.W., Freeman, M.F., Rhodes, C.S., Rowlands, G., 2001. Ambiguities in determination of self-affinity in the AE-index time series. Fractals 9, 471–479.
Williams, A.J., Lu, X.M., Slusher, B., Tortella, F.C., 2001. Electroencephalogram analysis and neuroprotective profile of the n-acetylated-α-linked acidic dipeptidase inhibitor, GPI5232, in normal and brain-injured rats. J. Pharmacol. Exp. Ther. 299, 48–57.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Spasic, S., Culic, M., Grbic, G. et al. Spectral and Fractal Analysis of Cerebellar Activity After Single and Repeated Brain Injury. Bull. Math. Biol. 70, 1235–1249 (2008). https://doi.org/10.1007/s11538-008-9306-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11538-008-9306-5