Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Abstract

The ability to respond selectively to particular frequency components of sensory inputs is fundamental to signal processing in the ear. The frog (Rana pipiens) sacculus, which is used for social communication and escape behaviors, is an exquisitely sensitive detector of sounds and ground-borne vibrations in the 5-to 200-Hz range, with most afferent axons having best frequencies between 40 and 60 Hz. We monitored the synaptic output of saccular sensory receptors (hair cells) by measuring the increase in membrane capacitance (⌬Cm) that occurs when synaptic vesicles fuse with the plasmalemma. Strong stepwise depolarization evoked an exocytic burst that lasted 10 ms and corresponded to the predicted capacitance of all docked vesicles at synapses, followed by a 20-ms delay before additional vesicle fusion. Experiments using weak stimuli, within the normal physiological range for these cells, revealed a sensitivity to the temporal pattern of membrane potential changes. Interrupting a weak depolarization with a properly timed hyperpolarization increased ⌬Cm. Small sinusoidal voltage oscillations (؎5 mV centered at ؊60 mV) evoked a ⌬Cm that corresponded to 95 vesicles per s at each synapse at 50 Hz but only 26 vesicles per s at 5 Hz and 27 vesicles per s at 200 Hz (perforated patch recordings). This frequency selectivity was absent for larger sinusoidal oscillations (؎10 mV centered at ؊55 mV) and was largest for hair cells with the smallest sinusoidal-stimulievoked Ca 2؉ currents. We conclude that frog saccular hair cells possess an intrinsic synaptic frequency selectivity that is saturated by strong stimuli.afferent ͉ synaptic vesicle pool ͉ ribbon synapse ͉ capacitance ͉ tuning T he auditory and vestibular systems in the ear and the related mechanosensory and electrosensory organs of the lateral line employ a remarkable variety of mechanical and neural mechanisms to distinguish frequency components of sensory signals from Ͻ10 Hz to nearly 100 kHz (1, 2). In each of these organs, a sensory stimulus passes through one or more stages of mechanical or electrical filtering (3), leading to graded changes in the sensory receptor cell's membrane potential, V m . Oscillatory sensory stimuli usually produce oscillations in V m , with the greatest amplitude occurring at a preferred frequency. Hair cells in the frog sacculus possess a broadly tuned electrical filter that causes V m to oscillate preferentially at frequencies between 35 and 75 Hz (4), as well as spontaneous oscillations of the mechanosensory apparatus at frequencies between 5 and 50 Hz (5).At the hair cells' output synapses, the information contained in V m is transmitted by a chemical neurotransmitter (glutamate) to postsynaptic terminals and encoded as a train of action potentials that travel to the brain. Each of these afferent synapses contains a presynaptic dense body [also known as the synaptic body (SB) or synaptic ribbon] (Fig. 1a) similar to ribbon synapses in the retina. As at other chemical synapses, V m controls calcium influx through voltage-gated cal...

Synaptic Ribbon Enables Temporal Precision of Hair Cell Afferent Synapse by Increasing the Number of Readily Releasable Vesicles: A Modeling Study

“…2, G and H, yellow-filled vesicles reveal a representative trial). This amount of exocytosis was within the range observed experimentally with capacitance measurements of hair cells from the frog sacculus after normalizing for differences in whole cell calcium current (Edmonds et al 2004;Rutherford and Roberts 2006).…”

Hair cell ribbon synapses

“…The relationship between structural and functional vesicle populations at ribbon-type active zones is still a matter of debate (for a review, see Nouvian et al 2006). There seems to be an agreement at least for mouse IHCs (Moser and Beutner 2000), turtle hair cells (Schnee et al 2005), and frog saccular hair cells (Rutherford and Roberts 2006) that the first exhaustible kinetic component (the RRP) corresponds to the docked vesicles (but, for an opposing view, see Edmonds et al 2004;Spassova et al 2004). …”

Structure and Function of the Hair Cell Ribbon Synapse

“…Hence, it is generally agreed that this component represents exocytosis of a small, finite pool of vesicles. Because it is the fastest discernible and exhaustible component of exocytosis several authors denominated it the readily releasable vesicle pool (RRP, Moser & Beutner, 2000; Spassova et al, 2004; Rutherford & Roberts, 2006) following the classical terminology of functional vesicle pools (Liley & North, 1953; Birks & MacIntosh 1961; Elmqvist & Quastel, 1965). Three major findings indicate that the first kinetic component is, indeed, involved in synaptic sound-coding by hair cells:

Correlation between the RRP size and the number of afferent synapses made by a hair cell as it varies along the tonotopic axis of the cochlea (Schnee et al, 2005).

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