Encoding of temporal features of auditory stimuli in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat

Abstract

Neurons in the superior paraolivary nucleus (SPON) respond to the offset of pure tones with a brief burst of spikes. Medial nucleus of the trapezoid body (MNTB) neurons, which inhibit the SPON, produce a sustained pure tone response followed by an offset response characterized by a period of suppressed spontaneous activity. This MNTB offset response is duration dependent and critical to the formation of SPON offset spikes (Kadner et al., 2006;Kulesza, Jr. et al., 2007). Here we examine the temporal resolution of the MNTB/SPON circuit by assessing its capability to i) detect gaps in tones, and ii) synchronize to sinusoidally amplitude modulated (SAM) tones. Gap detection was tested by presenting two identical pure tone markers interrupted by gaps ranging from 0-25 ms duration. SPON neurons responded to the offset of the leading marker even when the two markers were separated only by their ramps (i.e., a 0 ms gap); longer gap durations elicited progressively larger responses. MNTB neurons produced an offset response at gap durations of 2 ms or longer, with a subset of neurons responding to 0 ms gaps. SAM tone stimuli used the unit's characteristic frequency as a carrier, and modulation rates ranged from 40-1160 Hz. MNTB neurons synchronized to modulation rates up to ~1 KHz, whereas spiking of SPON neurons decreased sharply at modulation rates ≥ 400 Hz. Modulation transfer functions based on spike count were all-pass for MNTB neurons and low-pass for SPON neurons; the modulation transfer functions based on vector strength were low-pass for both nuclei, with a steeper cut-off for SPON neurons. Thus, the MNTB/SPON circuit encodes episodes of low stimulus energy, such as gaps in pure tones and troughs in amplitude modulated tones. The output of this circuit consists of brief SPON spiking episodes; their potential effects on the auditory midbrain and forebrain are discussed.

Development of on-off spiking in superior paraolivary nucleus neurons of the mouse

“…Although the accurate representation of temporal sound features is critically important for normal behavior in mammals, the neural mechanisms governing these processes are not fully understood. Growing evidence suggests that the superior paraolivary nucleus (SPON), a prominent cell group in the auditory brain stem (Kulesza et al 2002;Bazwinsky et al 2003;Kulesza 2008), may be specialized for encoding temporal information (Behrend et al 2002;Kulesza et al 2003;Kadner and Berrebi 2008;Felix et al 2011;Kopp-Scheinpflug et al 2011).…”

“…Transient spiking to the stimulus onset has also been reported (Behrend et al 2002;Dehmel et al 2002;Kulesza et al 2003); however, the prevalence of this response component as well as its role in SPON function remain unclear. In addition to pure tones, SPON neurons also respond to temporally complex stimuli, such as low rates of envelope amplitude modulation, with highly entrained spiking to individual modulation cycles (Behrend et al 2002;Kadner and Berrebi 2008). SPON neurons are also capable of signaling the presence of short gaps within ongoing sound stimuli (Kadner and Berrebi 2008).…”

“…In addition to pure tones, SPON neurons also respond to temporally complex stimuli, such as low rates of envelope amplitude modulation, with highly entrained spiking to individual modulation cycles (Behrend et al 2002;Kadner and Berrebi 2008). SPON neurons are also capable of signaling the presence of short gaps within ongoing sound stimuli (Kadner and Berrebi 2008). Thus, SPON neurons are well suited to faithfully transmit temporal information via their GABAergic projections to the inferior colliculus (IC), a major site of sensory integration located in the midbrain (Schofield 1991;Kulesza and Berrebi 2000;Saldaña and Berrebi 2000;Saldaña et al 2009).…”

The function of offset neurons in auditory information processing

“…When the inhibition accepted by offset neurons was discontinued, the offset response would change [80,81]. Therefore, we postulate a model which interprets this phenomenon (Fig.…”

“…The gap, or silent period, which is detectable between closely spaced sounds or components of sounds, is a vital sound character for sound communication of animals and human speech perception [81,[108][109][110].…”