Physiological Response Properties of Neurons in the Superior Paraolivary Nucleus of the Rat

Abstract

The superior paraolivary nucleus (SPON) is a prominent nucleus of the superior olivary complex. In rats, this nucleus is composed of a morphologically homogeneous population of GABAergic neurons that receive excitatory input from the contralateral cochlear nucleus and inhibitory input from the ipsilateral medial nucleus of the trapezoid body. SPON neurons provide a dense projection to the ipsilateral inferior colliculus and are thereby capable of exerting profound modulatory influence on collicular neurons. Despite recent interest in the structural and connectional features of SPON, little is presently known concerning the physiological response properties of this cell group or its functional role in auditory processing. We utilized extracellular, in vivo recording methods to study responses of SPON neurons to broad band noise, pure tone, and amplitude-modulated pure tone stimuli. Localization of recording sites within the SPON provides evidence for a medial (high frequency) to lateral (low frequency) tonotopic representation of frequencies within the nucleus. Best frequencies of SPON neurons spanned the audible range of the rat and receptive fields were narrow with V-shaped regions near threshold. Nearly all SPON neurons responded at the offset of broad band noise and pure tone stimuli. The vast majority of SPON neurons displayed very low rates of spontaneous activity and only responded to stimuli presented to the contralateral ear, although a small population showed binaural facilitation. Most SPON neurons also generated spike activity that was synchronized to sinusoidally amplitude-modulated tones. Taken together, these data suggest that SPON neurons may serve to encode temporal features of complex sounds, such as those contained in species-specific vocalizations.

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

“…In contrast to the medial and lateral superior olives, neurons in the rat SPON are monaurally driven and show no evidence of binaural interactions (Kulesza, Jr. et al, 2003Kadner et al, 2006), suggesting that the MNTB/SPON circuit encodes a stimulus feature other than sound source location. Based on current knowledge of its response properties, we hypothesized that this brainstem circuit may be particularly well suited for encoding stimulus features associated with episodes of low or rapidly decreasing sound energy, such as tone offsets and the falling flanks and troughs in SAM stimuli.…”

“…1A) (Kadner et al, 2006). The MNTB provides a strong glycinergic input to the nearby SPON (Helfert et al, 1989;Banks and Smith, 1992), whose neurons also display offset responses to pure tones; these however take the form of single or brief bursts of action potentials that occur after the stimulus offset (Fig 1B) (Kulesza, Jr. et al, 2003Kadner et al, 2006). Release from MNTB-derived glycinergic inhibition is critical to the formation of SPON offset responses, as demonstrated by reversible pharmacological blockade of glycine receptors in the SPON (Kulesza, Jr. et al, 2007).…”

“…Single unit responses from the medial nucleus of the trapezoid body (MNTB) and superior paraolivary nucleus (SPON) of the rat demonstrate that these two brainstem nuclei form a neural circuit producing duration dependent responses to the offset of pure tones and phase locked responses to SAM stimuli (Kulesza, Jr. et al, 2003Kadner et al, 2006). MNTB neurons display high rates of spontaneous activity and primary-like responses to characteristic frequency tones (cats: (Guinan, Jr. et al, 1972a, 1972bSmith et al, 1998), gerbils: (KoppScheinpflug et al, 2002), mice: (Kopp-Scheinpflug et al, 2003), rats: (Sommer et al, 1993;Paolini et al, 2001;Kulesza, Jr. et al, 2003;Kadner et al, 2006)).…”

“…MNTB neurons display high rates of spontaneous activity and primary-like responses to characteristic frequency tones (cats: (Guinan, Jr. et al, 1972a, 1972bSmith et al, 1998), gerbils: (KoppScheinpflug et al, 2002), mice: (Kopp-Scheinpflug et al, 2003), rats: (Sommer et al, 1993;Paolini et al, 2001;Kulesza, Jr. et al, 2003;Kadner et al, 2006)). The sustained excitatory response of MNTB units is followed by a period of suppressed spontaneous activity, sometimes lasting several tens of milliseconds, depending on stimulus parameters, that we refer to as the MNTB offset response (Fig.…”

Projections from auditory cortex contact ascending pathways that originate in the superior olive and inferior colliculus

“…The superior paraolivary nucleus in rats provides an important exception because virtually all the cells in this nucleus project to the IC (Saldaña and Berrebi, 2000). Kulesza et al (2003) characterized the acoustically-driven responses of single units in the rat superior paraolivary nucleus. They concluded that the cells in this nucleus are important for encoding temporal features of sounds.…”