The synaptic effects of ectopic spike initiation and the history dependence of axonal conduction
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1
New Jersey Institute of Technology, Biological Sciences, United States
Ectopic spike generation in the distal axonal sites has been studied for a number of decades (Bucher and Goaillard, 2011) but its importance in neural processing has only recently been examined (Kovalsky et al., 2009; Sheffield et al., 2011; Coggan et al., 2015). We explore the functional importance of ectopic spike generation in a motor axon involved in rhythm generation. The pyloric dilator (PD) neuron in the lobster Homarus americanus is one of the pacemaker neurons of the pyloric network in the stomatogastric nervous system. This neuron produces central bursting activity. If the central bursting is slow (< 1 Hz), in the presence of tonic (nanomolar) levels of dopamine (DA), the PD axon can produce tonic ectopic spikes (Bucher et al., 2003). DA also improve temporal fidelity in the PD axon, thus allowing all spikes within a burst to have similar conduction delay (Ballo et al., 2012). Both effects of DA result from activation of Ih in the PD axon, which leads to a depolarization of the baseline membrane potential (Ballo et al., 2010). These actions are counteracted by blockers of Ih.
We show that the rate of ectopic spiking increases if the central rhythmic bursting becomes slower. Consequently, if the central rhythm slows down, e.g. by the activity of the histaminergic pyloric suppressor neurons, the overall rate of spiking in PD is buffered by ectopic spiking in DA. The PD neurons targets two distinct muscles, cpv2a and cpv2b, which have, respectively, fast and slow EJPs. The presence of the tonic ectopic spikes greatly enhances the ability of the muscles, especially cpv2b, to produce a strong response to the centrally-generated bursting of the PD neuron. A simple computational model of the muscle response shows that the enhancement of the burst-induced EJPs in cpv2a by tonic ectopic spiking can result from short-term facilitation properties in this muscle.
In addition to the effects on ectopic spiking, DA, by improving temporal fidelity, leads to a more stable burst pattern (where the intraburst spike rate is more regular) at the axon terminals of the PD neuron. Although this effect is quite subtle (a few ms variation in spike timing within a 350 ms burst), the resulting EJP in the cpv2a and cpv2b muscles are significantly larger in response to this more stable burst pattern. In fact, the cpv2b response can increase to the point that it produces muscle action potential simply by stimulating the axon terminals with the DA-type burst pattern but not with the control burst pattern, even in the absence of DA.
Together, these results indicate a strong influence of DA tone modulation on the axon, by inducing ectopic spiking and stabilizing the intraburst spike rate, which can be important in determining the functional output of the neuron.
Acknowledgements
Supported by NIH NS083319.
References
Ballo AW, Nadim F, Bucher D (2012) Dopamine modulation of Ih improves temporal fidelity of spike propagation in an unmyelinated axon. J Neurosci 32:5106-5119.
Ballo AW, Keene JC, Troy PJ, Goeritz ML, Nadim F, Bucher D (2010) Dopamine modulates Ih in a motor axon. J Neurosci 30:8425-8434.
Bucher D, Goaillard JM (2011) Beyond faithful conduction: short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon. Prog Neurobiol 94:307-346.
Bucher D, Thirumalai V, Marder E (2003) Axonal dopamine receptors activate peripheral spike initiation in a stomatogastric motor neuron. J Neurosci 23:6866-6875.
Coggan JS, Sejnowski TJ, Prescott SA (2015) Cooperativity between remote sites of ectopic spiking allows afterdischarge to be initiated and maintained at different locations. J Comput Neurosci 39:17-28.
Kovalsky Y, Amir R, Devor M (2009) Simulation in sensory neurons reveals a key role for delayed Na+ current in subthreshold oscillations and ectopic discharge: implications for neuropathic pain. J Neurophysiol 102:1430-1442.
Sheffield ME, Best TK, Mensh BD, Kath WL, Spruston N (2011) Slow integration leads to persistent action potential firing in distal axons of coupled interneurons. Nat Neurosci 14:200-207.
Keywords:
Dopamine,
SPIKE INITIATION ZONE,
antidromic,
Neuromuscular Junction,
Stomatogastric
Conference:
Spike Initiation: Models & Experiments, Prague, Czechia, 22 Jul - 22 Jul, 2015.
Presentation Type:
Oral Presentation
Topic:
Neuroscience
Citation:
Daur
N,
Zhang
Y,
Nadim
F and
Bucher
DM
(2015). The synaptic effects of ectopic spike initiation and the history dependence of axonal conduction.
Front. Neurosci.
Conference Abstract:
Spike Initiation: Models & Experiments.
doi: 10.3389/conf.fnins.2015.90.00008
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Received:
15 Jul 2015;
Published Online:
16 Jul 2015.
*
Correspondence:
Dr. Farzan Nadim, New Jersey Institute of Technology, Biological Sciences, Newark, NJ, 07102, United States, farzan@njit.edu