Endogenous Firing Patterns of Murine Spiral Ganglion Neurons

Mo, Zun-Li and Robin L. Davis. Endogenous firing patterns of trical properties of the neurons themselves (Davis 1996; murine spiral ganglion neurons. J. Neurophysiol. 77: 1294–1305, Evans 1992; Javel 1986; Kiang 1990; Kiang et al. 1986; 1997. Current-clamp recordings with the use of the whole cell Ruggero 1992). Immunohistochemical localization of moleconfiguration of the patch-clamp technique were made from postcules such as neurofilaments (Romand et al. 1990), osteonatal mouse spiral ganglion neurons in vitro. Cultures contained pontin (Lopez et al. 1995), neuropeptide Y, and neuronneurons that displayed monopolar, bipolar, and pseudomonopolar specific enolase (Anniko et al. 1995) has further shown the morphologies. Additionally, a class of neurons having exceptioninherent complexity of the spiral ganglion. These molecules ally large somata was observed. Frequency histograms of the maxiare differentially localized to subclasses of primary auditory mum number of action potentials fired from 240-ms step depolarneurons that do not correspond to the type I/ type II categoriizations showed that neurons could be classified as either slowly adapting or rapidly adapting. Most neurons (85%) were in the zation. Some of these differences may be associated with rapidly adapting category (58 of 68 recordings) . Measurements of activity-regulated expression, such as that observed with Fos elementary properties were used to define the endogenous firing and Jun proteins (Morgan and Curran 1991); yet others characteristics of both neuron classes. Action potential number could be due to subtle subdivisions within the peripheral varied with step and holding potential, spike amplitude decayed innervation-based classification (Romand et al. 1990). during prolonged depolarizations, and spike frequency adaptation Although the molecular studies and in vivo electrophysiolwas observed in both rapidly and slowly adapting neurons. The ogy suggest that spiral ganglion neurons have nonuniform apparent input resistance, spike amplitude decrement, and instantacharacteristics that contribute differentially to the coding of neous firing frequency differed significantly between rapidly and auditory information, little is known about their endogenous slowly adapting neurons. Inward rectification was evaluated in refiring properties. This is a critical parameter to determine, sponse to hyperpolarizing constant current injections. Present in both electrophysiological classes, its magnitude was graded from because electrical signals from the periphery are shaped by neuron to neuron, reflecting differences in number, type, and/or postsynaptic membrane currents as well as by synaptic convoltage dependence of the underlying channels. These data suggest nections (Llinás 1988). On the basis of what is known about that spiral ganglion neurons possess intrinsic firing properties that primary neurons in other sensory systems (Perl 1992; regulate action potential number and timing, features that may be Shapley and Perry 1986), one would expect to observe discrucial to signal coding in the auditory periphery. tinct electrophysiological features that distinguish neurons within the auditory periphery that innervate different receptor types. I N T R O D U C T I O N To begin to address the issue of whether spiral ganglion neurons possess heterogeneous intrinsic firing patterns, we The sensory cells of the cochlea are innervated by two made whole cell current-clamp recordings from primary aumajor classes of primary auditory neurons that compose the ditory neurons separated from their peripheral targets in spiral ganglion. Type I neurons receive synaptic input from vitro. These studies showed unequivocally that postnatal muinner hair cells that mediate the initial stages of auditory rine primary auditory neurons do not display uniform reperception, whereas type II neurons, whose function is cursponses to injected currents. Instead, we identified two genrently unknown, innervate outer hair cells (Dallos 1992; eral neuron classes on the basis of action potential adaptaHudspeth 1989; Kelly 1991; Kiang 1984; Kiang et al. 1982; tion. The largest proportion of cells fired only a few spikes Kim 1984; Perkins and Morest 1975; Ryugo 1992; Spoendlin to a prolonged depolarization, thus adapting rapidly to the 1973). Thus, analogous to other sensory modalities such as stimulus. The remaining neurons fired multiple spikes, showthe somatosensory or visual systems, neurons that innervate ing slow adaptation. Other parameters, such as spike amplidifferent receptor types reside within the same ganglion. tude decrement, spike frequency adaptation, and inward recBeyond the two categories of spiral ganglion neurons, tification were examined in both neuronal classes and were which are based on peripheral innervation patterns, further found to be graded in magnitude. These results suggest that subclassifications have been observed. Electrophysiological subcategories of postnatal spiral ganglion neurons differenstudies have shown that type I neurons do not all display tially influence the time course and magnitude of the receptor identical firing properties in vivo. In addition to differences potential signals they transmit to the brain. in characteristic frequency, they show graded thresholds (Liberman 1978), differently shaped rate-intensity functions (Kiang et al. 1965; Winter et al. 1990), and a wide range M E T H O D S of spontaneous activity (Kiang et al. 1965; Liberman 1978; Tissue culture Schmiedt 1989) that can be classified into three discrete groups (Liberman 1978). These characteristics could result Spiral ganglia, removed from the surrounding cochlear tissues, from multiple sources, such as mechanical nonlinearities, were taken from neonatal CBA/J mice ranging in age from 1 to 6 postnatal days of development and were plated as explants in synaptic regulation of neuronal firing, and endogenous elec-