Connections of the Superior Paraolivary Nucleus of the Rat: II. Reciprocal Connections with the Tectal Longitudinal Column

Abstract

The superior paraolivary nucleus (SPON), a prominent GABAergic center of the mammalian auditory brainstem, projects to the ipsilateral inferior colliculus (IC) and sends axons through the commissure of the IC (CoIC). Herein we demonstrate that the SPON is reciprocally connected with the recently discovered tectal longitudinal column (TLC). The TLC is a long and narrow structure that spans nearly the entire midbrain tectum longitudinally, immediately above the periaqueductal gray matter (PAG) and very close to the midline. Unilateral injections of biotinylated dextran into the SPON of the rat label abundant terminal fibers in the TLC of both sides, with an ipsilateral predominance. The SPON provides a dense innervation of the entire rostrocaudal extent of the ipsilateral TLC, and a relatively sparser innervation of the caudal and rostral portions of the contralateral TLC. SPON fibers reach the TLC by two routes: as collaterals of axons of the CoIC, and as axons that circumvent the ipsilateral IC before traveling in the deep layers of the superior colliculus (SC). The density of these projections identifies SPON as a significant source of input to the TLC. Other targets of the SPON discovered in this study include the deep layers of the SC and the PAG. The same experiments reveal numerous labeled cell bodies in the TLC, interspersed among the labeled SPON fibers. This observation suggests that the SPON is a significant target of TLC projections. The discovery of novel reciprocal connections between the SPON and the TLC opens unexpected avenues for investigation of sound processing in mammalian brainstem circuits.

Auditory System

“…The SPO projects to the ipsilateral inferior colliculus and the tectal longitudinal column ( Fig. 3; Faye-Lund, 1986; Friauf and Kandler, 1990;Saldaña and Berrebi, 2000;Saldaña et al, 2009;Viñuela et al, 2011). Saldaña and Berrebi (2000) have described a topographic projection to the inferior colliculus, which strongly suggests that the SPO is tonotopically organized (Saldaña et al, 2009).…”

“…Many ascending afferents arise in the IC (Figs. 3, 14, 18 and 24;LeDoux et al, 1985aLeDoux et al, , 1987Oliver et al, 1999;Bartlett et al, 2000;Ito et al, 2009Ito et al, , 2011Oliver, 2010, 2012), and others originate in the CNC (Malmierca et al, 2002;Anderson et al, 2009), SOC and NLL (LeDoux et al, 1985aViñuela et al, 2011). These fibers enter the MG via the brachium of the inferior colliculus (Figs.…”

“…It projects to the ipsilateral inferior colliculus (Fig. 3;Friauf and Kandler, 1990;Saldaña and Berrebi, 2000;Saldaña et al, 2009;Aparicio et al, 2010;Viñuela et al, 2011) and may represent a hyperdevelopment of periolivary cells with a similar projection, present in smaller numbers in other mammals ( Fig. 9; cat: Adams, 1983a).…”

“…This group of neurons is referred to as the "tectal longitudinal column" or "TLC" and is made of GABAergic neurons (Vetter and Mugnaini, 1985), many of which have small cell bodies that are elongated; other medium-sized neurons with elongated or triangular somata also occur. The TLC is reciprocally interconnected with the the SPO and also received inputs from all IC subdivisions and (Saldaña et al, 2009;Aparicio et al, 2010;Viñuela et al, 2011) and may be a source of inhibitory inputs (Mugnaini and Oertel, 1985;Vetter and Mugnaini, 1985). The electrophysiological features of these neurons reveals that they possess broad frequency tuning, high threshold, long latencies, little synchronization or rate tuning to amplitude modulation frequency and a small degree of inhibition evoked by stimulation of the ipsilateral ear (Marshall et al, 2008).…”

Striking neuronal thymosin beta 4 expression in the deep layers of the mouse superior colliculus after monocular deprivation

“…Very recently, the tectal longitudinal column or TLC was discovered as a new nucleus in the rat, a narrow, elongated structure spanning the midbrain tectum longitudinally, now known to be present in a large variety of mammals (Saldaña et al 2007;Viñuela et al 2011). As found for the observed Tb4-immunoreactive neurons, this paired nucleus is located close to the midline, immediately dorsal to the periaqueductal gray matter and occupies what has traditionally been considered the most medial region of the deep superior colliculus and the most medial region of the inferior colliculus.…”