Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics

1. The discharge of peripheral otolith neurons in response to sinusoidal force variations was investigated in the barbiturate-anesthetized squirrel monkey (Saimiri sciureus). The sine waves were superimposed on a background force which biased the end organ so as to excite or inhibit the unit's firing. Both regularly and irregularly discharging neurons were studied. 2. The response amplitude, measured as a peak-to-peak changes in firing rate, reached near-maximal values during the first sine-wave cycle and, for most units, remained constant as sinusoidal stimulation was prolonged. 3. In regular units, introduction of an excitatory bias increased the sensitivity to sinusoidal stimulation in a manner consistent with the static asymmetries observed in the response to constant forces. Bias effects in irregular units were usually small and, in some cases, excitatory biases resulted in a decrease in sensitivity. 4. Variation in sine-wave amplitude had no effect on the sinusoidal gains or phases of regular units. For irregular units, there was some evidence of a small gain increase as stimulus amplitude decreased. 5. Nonlinear distortion was usually 10-20% and was mainly of an asymmetric type. In regular units, the distortion could be partially related to static asymmetries. 6. The response of regular units is predominantly tonic, that of irregular units more phasic. For regular units there was usually no more than a twofold gain enhancement as frequency was increased in the spectrum from DC to 2.0 Hz; typically, small phase leads at low frequencies were replaced by similar phase lags at higher frequencies. Irregular units were characterized by a 20-fold frequency-dependent gain enhancement over the same spectrum; phase leads of 20-40% were seen. 7. Bodeplots were fit by a family of transfer functions, each consisting of three terms. The first is a velocity-sensitive operator with a fractional exponent. The second is a low-frequency adaptation operator. Only the lag operator can be related to the dynamics of otoligh motion. Most of the variations among units, including those seen between regular and irregular units, can be accounted for by suitable variations in the velocity-sensitive and adaptation operators. 8. The transfer functions, when integrated and inverted, led to reasonable approximations of the response to force trapezoids. It is concluded that the transfer functions provide an adequate representation of the dynamic behavior of most units. The only exceptions are the few neurons showing delayed adaptation.