Cellular Mechanisms for Information Coding in Auditory Brain Stem Nuclei

Introduction The brain stem auditory nuclei carry out a wide variety of transformations of the signals carried by the auditory nerve. Although basic frequency and intensity information is first encoded in the cochlea, brain stem circuitry must perform further neural definitions and refinements of these parameters, as well as integrate the cues necessary for the localization of sounds in space. Each of these aspects is associated not just with certain cell types, morphologies, and synaptic connections, but with cells having characteristic electrical response profiles. Such response properties are an outcome of the complement of ion channels that the cells possess and of the dynamic properties of the synapses through which cells communicate. The link between the properties of channels, of synapses, and the higher-order functions of circuits is not simply correlative. Rather, we are beginning to understand the function of cellular and membrane properties in terms of the relationship between a given sound stimulus and the responses of the auditory nerve and different brain stem neurons in vivo. The cell types of the cochlear nuclei and superior olivary complex are numerous, and the full spectrum of their responses and functions is not yet clear. However, some key cell types have been well described and serve as excellent illustrations of the basic electrical themes. Auditory nerve fibers respond to simple acoustic stimuli with two general response profiles (Fig. 1; see Ruggero 1992). For low-frequency stimuli, nerve fibers fire action potentials or spikes in a phase-locked manner, i.e., with a spike occurring most often with a certain phase relationship to the sound stimulus. For high-frequency stimuli, responses show an initial peak at the onset of the sound, and then a rapid decline in firing rate down to a steady-state level of random (not phase-locked) activity. These responses are documented using a poststimulustime histogram (PSTH), in which the time of occurrence of spikes during repeated presentations of a stimulus is recorded (Fig. 1); such histograms illustrate at a glance the temporal relationship between the sound stimulus and the firing of the neuron. Recordings made from neurons in the auditory brain stem show characteristic levels of transformation of the primary afferent (auditory nerve) response pattern, and indeed these transformations are used in part to define the cell type. For example, postsynaptic neurons in the ventral cochlear nucleus (VCN) may respond almost identically to the activity patterns of the auditory nerve fibers; such responses are termed “primary-like” or PL (Pfeiffer 1966; Rhode 1986). Alternatively, neurons may show subtle or major deviations from this pattern. The goal of this chapter is explore how, at a membrane level, these firing patterns in postsynaptic cells might arise during synaptic activity. In the process, we will outline basic concepts in the physiology of ion channels and synapses as they relate to the function of auditory neurons.