Theoretical analysis of intercellular communication between the vestibular type I hair cell and its calyx ending

1. The vestibular type I hair cell and its calyx ending can communicate in three ways. 1) In conventional synaptic transmission an excitatory neurotransmitter is released in multimolecular packets from the hair cell and depolarizes the ending. 2) Ephaptic transmission occurs because currents originating in one structure change the membrane potential of the other structure. 3) Potassium is released from the hair cell during transduction, accumulates in the intercellular space, and can depolarize both the hair cell and the ending. 2. A system of steady-state cable equations was used to analyze conventional and ephaptic transmission. The equations describe the membrane potentials of the hair cell's basolateral surface and of the ending's inner and outer faces. A terminal resistor represents the apical pole of the hair cell and a second terminal resistor represents the parent fiber and other processes connected to the ending. Transducer currents are delivered to the hair cell at its apex and synaptic currents are delivered to the inner or outer faces of the ending at its base. 3. The presence of a calyx ending can reduce conventional synaptic transmission by lowering the postsynaptic input impedance and by introducing an intercellular component into the postsynaptic depolarization of the inner face. Transmission is expressed as a percentage of the synaptic depolarization that would occur in the absence of the ending. Increasing the specific resistance of the inner and outer faces from 150 to 15,000 omega.cm2 improves transmission almost tenfold, from 10% to > 90%. Selectively increasing the impedance of one or the other face results in only a twofold improvement. Under all conditions, transmission is similar for inner- and outer-face synaptic inputs. 4. Hair cell transducer currents cause an ephaptic hyperpolarization of the calyx inner face and a depolarization of the outer face. Excitatory postsynaptic currents originating in the calyx inner face hyperpolarize the apical part of the hair cell and depolarize its base. Outer-face excitatory currents depolarize the hair cell apex and hyperpolarize the base. On the basis of plausible assumptions about the magnitudes of input currents and about the electrical properties of the elements, it was estimated that ephaptic transmission to or from the inner face results in voltages of 0.5-2 mV in the target structure. Transmission to or from the outer face is 10-25 times less effective. 5. During transduction, K+ ions leave the hair cell's basolateral surface and accumulate in the intercellular space separating it from the calyx inner face. The accumulation was analyzed by combining cable and electrodiffusion theories. To make the theories consistent, the resistance of the intercellular space was derived from the Nernst-Planck equation. It was found that the steady-state intercellular current consisted of a diffusional and an electrical component. The diffusional component was 50-100 times larger than the electrical component. 6. Delta x[K+], the steady-state increase in intercellular K+ concentration from a baseline concentration of 4 mM, is proportional to IA, the magnitude of the transducer current, and is only slightly affected by the basolateral impedance. For a uniform distribution of basolateral currents, the proportionality constant, delta x[K+]/IA, is 0.07 mM/pA at the base and declines to 0 at the apex. A transducer current of 100 pA can result in a delta x[K+] of 7 mM at the base and a possible 25-mV depolarization of the hair cell and the ending. 7. Intercellular K+ accumulation has kinetics with a dominant rate constant of 12 s-1, corresponding to a first-order low-pass filter with a corner frequency of 2 Hz. Kinetics is sufficiently fast for accumulation to participate in the transduction of normally occurring head movements. (ABSTRACT TRUNCATED)