Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice

Abstract

1. Principal cells in the medial superior olive (MSO) receive low-frequency information from both ears via left and right cochlear nuclei. In vivo extracellular records suggest that some MSO neurons respond optimally only when the binaural acoustic signal has a precise interaural delay. Thus MSO cells, in particular principal cells, are thought to be the first stage in the processing of interaural time difference cues that provides information as to the location of a low-frequency sound in space. 2. Despite this proposed fundamental role for the MSO, certain features of this nucleus make in vivo recordings from any cell type here very difficult to obtain. Only a small number of extracellular records and no intracellular recordings are reported in the literature. Using sharp, neurobiotin-filled glass electrodes to record intracellularly from cells in an in vitro brain slice of the guinea pig superior olivary complex, I have begun to assess the anatomic and physiological features of cells in the MSO that might be relevant to such a functional role in vivo. 3. Two basic MSO cell types, designated principal and nonprincipal, could be distinguished on the basis of certain anatomic and physiological differences. 4. Labeled principal cell bodies were located at all dorsoventral location within the MSO. Labeled nonprincipal cells were located in or around the dorsal aspects of the nucleus. Principal cells typically had thick bipolar dendrites (1 directed medially, 1 laterally) that did not taper or branch significantly except at their terminations. Nonprincipal cells were multipolar with three to nine thinner primary dendrites that did not branch preferentially in a mediolateral direction. Principal cell axons gave off collaterals terminating in and around the dorsal MSO. Nonprincipal cells also had axon in and around the dorsal MSO. Nonprincipal cells also had axon collateral branches innervating dorsal MSO, but these axons could branch more extensively and project further down the dorsoventral aspect of the nucleus. 5. Principal cells typically responded to depolarizing current pulses with one or a few spikes at current onset. When bathed in saline containing 4-aminopyridine (4-AP), they fired repetitively to the same depolarizing current pulses. This would indicate a depolarization-induced nonlinearity similar to that seen in principal cell types of two other auditory brain stem nuclei, the anteroventral cochlear nucleus and medial nucleus of the trapezoid body. Nonprincipal cells normally fired repetitively to depolarizing current pulses even close to spike threshold. Both cell types could show a sag in the membrane potential to hyperpolarizing current pulses.(ABSTRACT TRUNCATED AT 400 WORDS)

Cross Correlation by Neurons of the Medial Superior Olive: a Reexamination

“…Yet another possibility is that inhibition occurs at ITDs at which binaural coincidences do not, counteracting the dispersive effects of monaural coincidences. There is ample evidence that inhibitory inputs are present and functional (Adams and Mugnaini 1990;Banks and Smith 1992;Brand et al 2002;Cant and Hyson 1992;Covey et al 1991;Sanes 1993, 1994;Kiss and Majorossy 1983;Kuwabara and Zook 1992;Smith 1995;Spangler et al 1985).…”

Modeling Binaural Responses in the Auditory Brainstem to Electric Stimulation of the Auditory Nerve

“…Using a multicompartment model of avian NL, Agmon-Snir et al (1998) showed that the systematic dependence of dendritic length on tonotopic position observed in chick NL (Smith and Rubel 1979) is essential to obtain good ITD tuning over a wide range of frequencies. While our single compartment model cannot address the effects of cellular morphology on coincidence detection, there is no evidence for a tonotopic gradient in dendritic length or synaptic input strength in mammalian MSO (Henkel and Brunso-Bechtold 1990;Smith 1995). Using a gerbil MSO slice preparation, Mathews et al (2010) demonstrated that a gradient of G KLT along the dendrites of MSO neurons increased the modulation of rate-ITD curves.…”

“…Similarly, single neurons in the inferior colliculus (IC) of acutely deafened cats can exhibit good ITD sensitivity to electric pulse trains at low pulse rates (G100 pps) for moderate stimulus levels, but their ITD sensitivity degrades at higher pulse rates where many neurons show only an onset response (Smith andDelgutte 2007, 2008;Hancock et al 2012). The narrow range of pulse rates yielding good ITD sensitivity with electric stimulation in deaf animals contrasts with the wider range of frequencies over which ITD sensitivity to pure tones is observed in normal hearing animals in both the medial superior olive (MSO) (Yin and Chan 1990) and the IC (Kuwada and Yin 1983;Kuwada et al 1987).…”

Neural Sensitivity to Periodicity in the Inferior Colliculus: Evidence for the Role of Cochlear Distortions

“…Peaks in the PSTH indicate a 1-Hz modulation in the neuron's discharge pattern (3 complete response cycles over the 3-s stimulus presentation). The rate of the response modulation equates to the difference between the pure-tone frequency in one ear and the AM rate in the other, suggesting the possibility that it results from binaural integration of temporally phase-locked inputs, a process usually considered to arise in the medial superior olive of the brain stem, below the level of the IC, and that requires specialized cell types (Smith 1995;Smith et al 1998) and synaptic mechanisms (Agmon-Snir et al 1998; Forsythe and Barnes-Davies 1993) considered unique to the lower binaural brain stem. Figure 2 shows the responses of another IC neuron, with an audio-visually determined CF of 364 Hz, to low-frequency pure tones and high-frequency AM tones.…”