Non-random nature of spontaneous mIPSCs in mouse auditory brainstem neurons revealed by recurrence quantification analysis
Abstract
A change in the spontaneous release of neurotransmitter is a useful indicator of processes occurring within presynaptic terminals. Linear techniques (e.g. Fourier transform) have been used to analyse spontaneous synaptic events in previous studies, but such methods are inappropriate if the timing pattern is complex. We have investigated spontaneous glycinergic miniature synaptic currents (mIPSCs) in principal cells of the medial nucleus of the trapezoid body. The random versus deterministic (or periodic) nature of mIPSCs was assessed using recurrence quantification analysis. Nonlinear methods were then used to quantify any detected determinism in spontaneous release, and to test for chaotic or fractal patterns. Modelling demonstrated that this procedure is much more sensitive in detecting periodicities than conventional techniques. mIPSCs were found to exhibit periodicities that were abolished by blockade of internal calcium stores with ryanodine, suggesting calcium oscillations in the presynaptic inhibitory terminals. Analysis indicated that mIPSC occurrences were chaotic in nature. Furthermore, periodicities were less evident in congenitally deaf mice than in normal mice, indicating that appropriate neural activity during development is necessary for the expression of deterministic chaos in mIPSC patterns. We suggest that chaotic oscillations of mIPSC occurrences play a physiological role in signal processing in the auditory brainstem.
References
Abenavoli A, Forti L, Bossi M, Bergamaschi A, Villa A& Malgaroli A . 2002Multimodal quantal release at individual hippocampal synapses: evidence for no lateral inhibition. J. Neurosci. 22, 6336–6346. Crossref, PubMed, ISI, Google Scholar- Bacchereti, M. 2004 Analisi quantitativa delle recurrence plots: RQA2 in: Sviluppo di modelli non lineari per l'analisi di segnali elettroencefalografici. Ph.D. thesis, Universita di Pisa. Google Scholar
Bock G.R, Frank M.P& Steel K.P . 1982Preservation of central auditory function in the deafness mouse. Brain Res. 39, 608–612.doi:10.1016/0006-8993(82)90536-4. . Crossref, ISI, Google ScholarClements J.D& Bekkers J.M . 1997Detection of spontaneous synaptic events with an optimally scaled template. Biophys. J. 73, 220–229. Crossref, PubMed, ISI, Google ScholarCollin T, Marty A& Llano I . 2005Presynaptic calcium stores and synaptic transmission. Curr. Opin. Neurobiol. 15, 275–281.doi:10.1016/j.conb.2005.05.003. . Crossref, PubMed, ISI, Google ScholarEmptage N.J, Reid C.A& Fine A . 2001Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron. 29, 197–208.doi:10.1016/S0896-6273(01)00190-8. . Crossref, PubMed, ISI, Google ScholarFadel P.J, Barman S.M, Phillips S.W& Gebber G.L . 2004Fractal fluctuations in human respiration. J. Appl. Physiol. 97, 2056–2064. Crossref, PubMed, ISI, Google ScholarFaure P& Korn H . 1997A non-random dynamic component in the synaptic noise of a central neuron. Proc. Natl Acad. Sci. USA. 94, 6506–6511.doi:10.1073/pnas.94.12.6506. . Crossref, PubMed, ISI, Google ScholarFilligoi G& Felici F . 1999Detection of hidden rhythms in surface EMG signals with a non-linear time-series tool. Med. Eng. Phys. 21, 439–448.doi:10.1016/S1350-4533(99)00073-9. . Crossref, PubMed, ISI, Google ScholarKriebel M.E& Bridy D.J . 1996Dynamics of ethanol-induced transmitter release in the frog neuromuscular junction. Brain Res. 729, 228–233.doi:10.1016/0006-8993(96)00425-8. . Crossref, PubMed, ISI, Google ScholarLeao R.N, Oleskevich S, Sun H, Bautista M, Fyffe R.E& Walmsley B Differences in glycinergic mIPSCs in the auditory brain stem of normal and congenitally deaf neonatal mice. J. Neurophysiol. 91, 2004a1006–1012.doi:10.1152/jn.00771.2003. . Crossref, PubMed, ISI, Google ScholarLeao R.N, Berntson A, Forsythe I.D& Walmsley B Reduced low-voltage activated K+ conductance and enhanced central excitability in a congenitally deaf (dn/dn) mouse. J. Physiol. 559, 2004b25–33.doi:10.1113/jphysiol.2004.067421. . Crossref, PubMed, ISI, Google ScholarLim R, Oleskevich S, Few A.P, Leao R.N& Walmsley B . 2003Glycinergic mIPSCs in mouse and rat brainstem auditory nuclei: modulation by ruthenium red and the role of calcium stores. J. Physiol. 546, 691–699.doi:10.1113/jphysiol.2002.035071. . Crossref, PubMed, ISI, Google ScholarLlano I, Gonzalez J, Caputo C, Lai F.A, Blayney L.M, Tan Y.P& Marty A . 2000Presynaptic calcium stores underlie large amplitude miniature IPSCs and spontaneous calcium transients. Nat. Neurosci. 3, 1256–1265.doi:10.1038/81781. . Crossref, PubMed, ISI, Google ScholarLohmann C, Finski A& Bonhoeffer T . 2005Local calcium transients regulate the spontaneous motility of dendritic filopodia. Nat. Neurosci. 8, 305–312.doi:10.1038/nn1406. . Crossref, PubMed, ISI, Google ScholarLowen S.B, Casg S.S, Poo M& Teich M.C . 1997Quantal neurotransmitter secretion rate exhibits fractal behavior. J. Neurosci. 17, 5666–5677. Crossref, PubMed, ISI, Google ScholarMeiri H& Rahamimoff R . 1978Clumping and oscillations in evoked transmitter release at the frog neuromuscular junction. J. Physiol. 278, 513–523. Crossref, PubMed, ISI, Google ScholarMelamed N, Helm P.J& Rahamimoff R . 1993Confocal microscopy reveals coordinated calcium fluctuations and oscillations in synaptic boutons. J. Neurosci. 13, 632–649. Crossref, PubMed, ISI, Google ScholarNieminen H& Takala E.P . 1996Evidence of deterministic chaos in the myoelectric signal. Electromyogr. Clin. Neurophys. 36, 49–58. PubMed, Google ScholarOleskevich S& Walmsley B . 2002Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice. J. Physiol. 540, 447–455.doi:10.1113/jphysiol.2001.013821. . Crossref, PubMed, ISI, Google ScholarPawson P.A& Grinnell A.D . 1989Oscillation period of MEPP frequency at frog neuromuscular junctions is inversely correlated with release efficacy and independent of acute Ca2+ loading. Proc. R. Soc. B. 237, 489–499. Link, ISI, Google ScholarRosenstein M.T, Collins J.J& De Luca C.J . 1993A practical method for calculating largest Lyapunov exponents from small data sets. Physica D. 65, 117–134. Crossref, ISI, Google ScholarSchweighofer N, Doya K, Fukai H, Chiron J.V, Furukawa T& Kawato M . 2004Chaos may enhance information transmission in the inferior olive. Proc. Natl Acad. Sci. USA. 101, 4655–4660.doi:10.1073/pnas.0305966101. . Crossref, PubMed, ISI, Google ScholarSharma G& Vijayaraghavan S . 2003Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron. 38, 929–939.doi:10.1016/S0896-6273(03)00322-2. . Crossref, PubMed, ISI, Google ScholarSimkus C.R& Stricker C . 2002The contribution of intracellular calcium stores to mEPSCs recorded in Layer II neurones of rat barrel cortex. J. Physiol. 545, 521–535.doi:10.1113/jphysiol.2002.022103. . Crossref, PubMed, ISI, Google ScholarSpitzer N.C . 2002Activity-dependent neuronal differentiation prior to synapse formation: the functions of calcium transients. J. Physiol. Paris. 96, 73–80.doi:10.1016/S0928-4257(01)00082-1. . Crossref, PubMed, Google ScholarSpitzer N.C, Lautermilch N.J, Smith R.D& Gomez T.M . 2000Coding of neuronal differentiation by calcium transients. Bioessays. 22, 811–817.doi:10.1002/1521-1878(200009)22:9<811::AID-BIES6>3.0.CO;2-G. . Crossref, PubMed, ISI, Google ScholarVan der Kloot W, Andricioaei I& Balezina O.P . 1999Examining the timing of miniature endplate potential releases at the frog and mouse neuromuscular junctions for deviations from Poisson expectations. Pflug. Arch.: Eur. J. Physiol. 438, 578–586.doi:10.1007/s004240051080. . Crossref, PubMed, ISI, Google ScholarVan Helden D.F& Zhao J . 2000Lymphatic vasomotion. Clin. Exp. Pharmacol. Physiol. 27, 1014–1018.doi:10.1046/j.1440-1681.2000.03368.x. . Crossref, PubMed, ISI, Google ScholarZbilut J.P, Thomasson N& Webber C.L . 2000Recurrence quantification analysis as a tool for nonlinear exploration of nonstationary cardiac signals. Med. Eng. Phys. 24, 52–60. ISI, Google Scholar



