Abstract
Using methods of geometric dynamical systems modeling, we demonstrate the mechanism through which inhibitory feedback synapses to oscillatory neurons stabilize the oscillation, resulting in a flattened phase-resetting curve. In particular, we use the concept of a synaptic phase-resetting curve to demonstrate that periodic inhibitory feedback to an oscillatory neuron locks at a stable phase where it has no impact on cycle period and yet it acts to counter the effects of extrinsic perturbations. These results are supported by data from the stable bursting oscillations in the crustacean pyloric central pattern generator.
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Notes
- 1.
\(\epsilon {v}^{{\prime}} = ({i}_{\mathrm{ext}}-{i}_{L}-{i}_{\mathrm{Ca}}-{i}_{\mathrm{syn}})/{c}_{m};\, {m}_{8}(v) = 1/(1+\exp (-(v+61)/4.2));\, {h}_{8}(v) = 1/(1+\exp ((v+88)/8.6));\, {\tau }_{h}(v) = (270/(1+\exp ((v +84)/7.3)))(\exp ((v +162)/30.0))+54;\, {i}_{\mathrm{ext}} = -0.45,\,{g}_{L} = 0.3142,\,{g}_{\mathrm{Ca}} = 1.2567,{g}_{\mathrm{syn}} = 0.0235\)(active for 219.4 ms starting at t 0 = 302 ms in each cycle), \({E}_{L} = -62.5,{E}_{\mathrm{Ca}} = 120,{E}_{\mathrm{syn}} = -80,{c}_{m} = 7,\epsilon = 1.\)
References
Achuthan, S., & Canavier, C. C. (2009). Phase-resetting curves determine synchronization, phase locking, and clustering in networks of neural oscillators. J Neurosci, 29(16), 5218–5233. doi: 29/16/5218 [pii] 10.1523/JNEUROSCI.0426–09.2009
Bartos, M., Vida, I., & Jonas, P.(2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci, 8(1), 45–56. doi: nrn2044 [pii] 10.1038/nrn2044
Borgers, C., & Kopell, N.(2003). Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity. Neural Comput, 15(3), 509–538. doi: 10.1162/089976603321192059
Brown, E., Moehlis, J., Holmes, P., Clayton, E., Rajkowski, J., & Aston-Jones, G.(2004). The influence of spike rate and stimulus duration on noradrenergic neurons. J Comput Neurosci, 17(1), 13–29. doi: 10.1023/B:JCNS.0000023867.25863.a4 5273291 [pii]
Dickinson, P. S.(2006). Neuromodulation of central pattern generators in invertebrates and vertebrates. Curr Opin Neurobiol, 16(6), 604–614. doi: S0959–4388(06)00148–6 [pii] 10.1016/j.conb.2006.10.007
Ermentrout, Bard.(2002). Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students. Philadelphia: Society for Industrial and Applied Mathematics.
Ermentrout, Bard, & Terman, David H.(2010). Mathematical foundations of neuroscience. New York: Springer.
Friesen, W. O.(1994). Reciprocal inhibition: a mechanism underlying oscillatory animal movements. Neurosci Biobehav Rev, 18(4), 547–553.
Grillner, S., Markram, H., De Schutter, E., Silberberg, G., & LeBeau, F. E.(2005). Microcircuits in action–from CPGs to neocortex. Trends Neurosci, 28(10), 525–533. doi: S0166–2236(05)00211–0 [pii] 10.1016/j.tins.2005.08.003
Guckenheimer, John, & Holmes, Philip.(1997). Nonlinear oscillations, dynamical systems, and bifurcations of vector fields(Corr. 5th print. ed.). New York: Springer.
Kintos, N., Nusbaum, M. P., & Nadim, F.(2008). A modeling comparison of projection neuron- and neuromodulator-elicited oscillations in a central pattern generating network. J Comput Neurosci, 24(3), 374–397. doi: 10.1007/s10827–007–0061–7
Mamiya, A., & Nadim, F.(2004). Dynamic interaction of oscillatory neurons coupled with reciprocally inhibitory synapses acts to stabilize the rhythm period. J Neurosci, 24(22), 5140–5150.
Manor, Y., Nadim, F., Epstein, S., Ritt, J., Marder, E., & Kopell, N. (1999). Network oscillations generated by balancing graded asymmetric reciprocal inhibition in passive neurons. J Neurosci, 19(7), 2765–2779.
Marder, E., & Calabrese, R. L.(1996). Principles of rhythmic motor pattern generation. Physiol Rev, 76(3), 687–717.
Mishchenko, E., & Rozov, N.(1997). Differential Equations with Small Parameters and Relaxation Oscillations. New York: Plenum Press.
Oprisan, S. A., Thirumalai, V., & Canavier, C. C.(2003). Dynamics from a time series: can we extract the phase resetting curve from a time series? Biophys J, 84(5), 2919–2928. doi: S0006–3495(03)70019–8 [pii] 10.1016/S0006–3495(03)70019–8
Pinsker, H. M.(1977). Aplysia bursting neurons as endogenous oscillators. I. Phase-response curves for pulsed inhibitory synaptic input. J Neurophysiol, 40(3), 527–543.
Prinz, A. A., Thirumalai, V., & Marder, E.(2003). The functional consequences of changes in the strength and duration of synaptic inputs to oscillatory neurons. J Neurosci, 23(3), 943–954.
Somers, D., & Kopell, N.(1993). Rapid synchronization through fast threshold modulation. Biol Cybern, 68(5), 393–407.
Thirumalai, V., Prinz, A. A., Johnson, C. D., & Marder, E.(2006). Red pigment concentrating hormone strongly enhances the strength of the feedback to the pyloric rhythm oscillator but has little effect on pyloric rhythm period. J Neurophysiol, 95(3), 1762–1770.
Wang, X. J., & Buzsaki, G.(1996). Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci, 16(20), 6402–6413.
Whittington, M. A., Traub, R. D., Kopell, N., Ermentrout, B., & Buhl, E. H.(2000). Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol, 38(3), 315–336. doi: S0167876000001732 [pii]
Zhou, L., LoMauro, R. and Nadim, F.(2006). The interaction between facilitation and depression of two release mechanisms in a single synapse. Neurocomputing, 69, 1001–1005.
Acknowledgements
We thank Dr. Lian Zhou for earlier ideas on this work. Supported by NIH MH-60605 (FN), NSF DMS0615168 (AB) and a Fulbright–Nehru Fellowship (AB).
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Nadim, F., Zhao, S., Bose, A. (2012). A PRC Description of How Inhibitory Feedback Promotes Oscillation Stability. In: Schultheiss, N., Prinz, A., Butera, R. (eds) Phase Response Curves in Neuroscience. Springer Series in Computational Neuroscience, vol 6. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0739-3_16
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DOI: https://doi.org/10.1007/978-1-4614-0739-3_16
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