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Inhibition of presynaptic Na(+)/K(+)-ATPase reduces readily releasable pool size at the avian end-bulb of Held synapse.

Department of Molecular Cell Physiology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan.
Neuroscience Research (Impact Factor: 2.2). 11/2011; 72(2):117-28. DOI: 10.1016/j.neures.2011.11.003
Source: PubMed

ABSTRACT A glutamatergic end-bulb synapse in the avian nucleus magnocellularis relays temporal sound information from the auditory nerve. Here, we show that presynaptic Na(+)/K(+)-ATPase (NKA) activity at this synapse contributes to the maintenance of the readily releasable pool (RRP) of vesicles, thereby preserving synaptic strength. Whole-cell voltage clamp recordings were made from chick brainstem slices to examine the effects of NKA blocker dihydroouabain (DHO) on synaptic transmission. DHO suppressed the amplitude of EPSCs in a dose-dependent manner. This suppression was caused by a decrease in the number of neurotransmitter quanta released because DHO increased the coefficient of variation of EPSC amplitude and reduced the frequency but not the amplitude of miniature EPSCs. Cumulative plots of EPSC amplitude during a stimulus train revealed that DHO reduced the RRP size without affecting vesicular release probability. DHO did not affect [Ca(2+)](i)-dependent processes, such as the paired-pulse ratio or recovery time course from the paired-pulse depression, suggesting a minimal effect on Ca(2+) concentration in the presynaptic terminal. Using mathematical models of synaptic depression, we further demonstrated the contribution of RRP size to the synaptic strength during a high-frequency stimulus train to highlight the importance of presynaptic NKA in the auditory synapse.

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    ABSTRACT: In the auditory system, sounds are processed in parallel frequency-tuned circuits, beginning in the cochlea. Activity of auditory nerve fibers reflects this frequency-specific topographic pattern, known as tonotopy, and imparts frequency tuning onto their postsynaptic target neurons in the cochlear nucleus. In birds, cochlear nucleus magnocellularis (NM) neurons encode the temporal properties of acoustic stimuli by "locking" discharges to a particular phase of the input signal. Physiological specializations exist in gradients corresponding to the tonotopic axis in NM that reflect the characteristic frequency (CF) of their auditory nerve fiber inputs. One feature of NM neurons that has not been investigated across the tonotopic axis is short-term synaptic plasticity. NM offers a rather homogeneous population of neurons with a distinct topographical distribution of synaptic properties that is ideal for the investigation of specialized synaptic plasticity. Here we demonstrate for the first time that short-term synaptic depression (STD) is expressed topographically, where unitary high CF synapses are more robust with repeated stimulation. Correspondingly, high CF synapses drive spiking more reliably than their low CF counterparts. We show that postsynaptic AMPA receptor desensitization does not contribute to the observed difference in STD. Further, rate of recovery from depression, a presynaptic property, does not differ tonotopically. Rather, we show that another presynaptic feature, readily releasable pool (RRP) size, is tonotopically distributed and inversely correlated with vesicle release probability. Mathematical model results demonstrate that these properties of vesicle dynamics are sufficient to explain the observed tonotopic distribution of STD.
    Journal of Neuroscience 01/2014; 34(4):1314-24. · 6.91 Impact Factor

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