Miniature EPSPs and Sensory Encoding in the Primary Afferents of the Vestibular Lagena of the Toadfish, Opsanus tau

Abstract

The synaptic activity transmitted from vestibular hair cells of the lagena to primary afferent neurons was recorded in vitro using sharp, intracellular microelectrodes. At rest, the activity was composed of miniature excitatory postsynaptic potentials (mEPSPs) at frequencies from 5 to 20/s and action potentials (APs) at frequencies betwen 0 and 10/s. mEPSPs recorded from a single fiber displayed a large variability. For mEPSPs not triggering APs, amplitudes exhibited an average coefficient of variance (CV) of 0.323 and rise times an average CV of 0.516. APs were only triggered by mEPSPs with larger amplitudes (estimated 4-6 mV) and/or steeper maximum rate of rise (10.9 mV/ms, +/- 3.7 SD, n=4 experiments) compared to (3.50 mV/ms, +/-0.07 SD, n=6 experiments) for nontriggering mEPSPs. The smallest mEPSPs showed a fast rise time (0.99 ms between 10% and 90% of peak amplitude) and limited variability across fibers (CV:0.18) confirming that they were not attenuated signals, but rather represented single-transmitter discharges (TDs). The mEPSP amplitude and rise-time relationship suggests that many mEPSPs represented several, rather than a single pulse of secretion of TDs. According to the estimated overall TD frequency, the coincidence of TDs contributing to the same mEPSP were not statistically independent, indicating a positive interaction between TDs that is reminiscent of the way subminiature signals group to form miniature signals at the neuromuscular junction. Depending on the duration and intensity of efferent stimulation, a complete block of AP initiation occurred either immediately or after a delay of a few seconds. Efferent stimulation did not significantly change AP threshold level, but abruptly decreased mEPSP frequency to a near-complete block that followed the block of APs. Maximum mEPSP rate of rise decreased during, and recovered progressively after, efferent stimulation. After termination of efferent stimulation, mEPSP amplitude did not recover instantly and for a few seconds the amplitude distribution of synaptic events showed fewer large-amplitude events than during the control period. This confirms that mEPSP amplitude and rate of rise properties, which are critical for triggering afferent APs, are modified by efferent activity. The depression of afferent AP firing during efferent stimulation corresponded to a decrease in mEPSP frequency and, to a lesser extent, a decrease in mEPSP amplitude and rate of rise, suggesting, a decrease in the level of interaction among TDs contibuting to a mEPSP.

The Unitary Event Underlying Multiquantal EPSCs at a Hair Cell's Ribbon Synapse

“…The usual response of about −130 pA implies the release of transmitter equivalent to two or three quanta; the largest events, about −300 pA in magnitude, correspond to the synchronous exocytosis of five or six quanta. Because we detected no temporal substructure in the waveforms of large events, we do not have evidence that they arise from independent vesicle fusions and cannot distinguish among three candidate mechanisms for the production of such signals: highly synchronous, cooperative fusion at distinct docking sites (Locke et al, 1999; Singer et al, 2004); compound fusion, in which several vesicles fuse together before undergoing exocytosis at a single site (Edmonds et al, 2004; Matthews and Sterling, 2008); and cumulative fusion, in which exocytosis by one docked vesicle initiates the rapid, piggyback fusion of several additional ones stacked along the ribbon (Hafez et al, 2003). …”

A review of synaptic mechanisms of vestibular efferent signaling in turtles: Extrapolation to efferent actions in mammals

“…These associations, however, are likely coincidental and three arguments may be provided: (1) Afferent responses are not qualitatively different when stimulating different groups of vestibular efferent neurons in the brainstem (i.e. contralateral vs. ipsilateral) [6,24,50]; (2) Canal afferents in the toadfish respond similarly to stimulation of efferent neurons either in the brainstem or along peripheral branches [6,28]; and (3) Brainstem stimulation in the toadfish excites canal afferents but inhibits afferents innervating the lagena [6,43]. Together, these observations suggest that the sources of different efferent actions are distal to the site of efferent stimulation.…”

Mechanisms of Efferent-Mediated Responses in the Turtle Posterior Crista

“…In comparison, although we know a great deal about efferent effects on spike discharge in vestibular organs (Goldberg et al, 1999), studies of the corresponding cellular mechanisms have been limited. Afferent recordings show that efferent excitation and inhibition in frog vestibular organs (Rossi et al, 1980;Sugai et al, 1991), as well as inhibition in the toadfish lagena (Locke et al, 1999), are correlated with changes in quantal rate arising from hair cells. Inhibition in the frog saccular macula, a vibratory organ, is consistent with the sequential activation of ␣9/␣10 and SK channels (Sugai et al, 1992;Holt et al, 2001;Rothlin et al, 2003).…”