Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections

Abstract

To ascertain whether the auditory neocortex also innervates the central nucleus of the inferior colliculus (CNIC) and not only its dorsal (DCIC) and external (ECIC) cortices, the anterograde tracers Phaseolus vulgaris-leucoagglutinin (PHA-L) and biotinylated dextran (BD) were injected into the primary auditory neocortex of albino rats (Te1), and labeled corticocollicular fibers were studied via light and electron microscopy. Axons from discrete regions of Te1 form two rostrocaudally oriented laminar plexuses of terminal fibers in the ipsilateral inferior colliculus (IC) and one in the contralateral IC. The first ipsilateral plexus, located in the medial half of the IC, has a dorsomedial to ventrolateral orientation, parallel to the isofrequency planes of the IC; is continuous through the CNIC and DCIC; and extends into the rostral ECIC. The second plexus is located in the deep layers of the lateral ECIC. These two plexuses meet caudally and ventrally, at the border between the CNIC and the lateral ECIC. The plexus in the contralateral IC is less dense and shorter than the two ipsilateral plexuses and is symmetric to the medial plexus. The thickness of the three plexuses is correlated with the size of the injection site, and their mediolateral and dorsoventral positions change as the injection site in Te1 is displaced rostrocaudally, with more caudal injections resulting in more dorsolateral medial plexuses and more dorsomedial lateral plexuses. Furthermore, the ventromedial border of the IC receives nontopographic, convergent projections from wide regions of rostral portions of Te1. The distribution of these corticocollicular plexuses mimics the topography of previously described intracollicular fibers. Electron microscopy shows that, in all three subdivisions of the ipsilateral IC, corticocollicular fibers form small boutons with features generally associated with excitatory transmission; i.e., they contain round synaptic vesicles and form asymmetric synapses with thin dendritic shafts and spines. These results demonstrate that the auditory corticocollicular projections innervate more extensive regions of the IC than were previously observed. Although peripheral regions receive the densest projection, the entire IC appears to be the target of corticofugal input.

The TLC: A Novel Auditory Nucleus of the Mammalian Brain

“…4 A-D, 7A-D]. Shortly thereafter, Saldaña et al (1996) noticed terminal fields in the same location formed by collaterals of auditory corticocollicular fibers that crossed the CoIC [Saldaña et al (1996), their Fig. 9 B, C].…”

“…In the rat, the TLC is innervated by the IC (Saldaña and Merchán, 1992) and by the auditory neocortex (Saldaña et al, 1996), and similar connectivity is apparent in the cat (Morest and Oliver, 1984). Moreover, the TLC is crossed by the CoIC, which includes projections from yet additional auditory structures, including the superior paraolivary nucleus, the sagulum and the nuclei of the lateral lemniscus (Saldaña and Merchán, 2005).…”

Efficient Encoding of Vocalizations in the Auditory Midbrain

“…The IC is the main nucleus in the auditory midbrain, receiving ascending input from the majority of brainstem nuclei (Adams, 1979) and descending projections from auditory cortex (Saldaña et al, 1996). Efficient encoding of conspecific vocalizations may be facilitated by neurons in the IC that respond to specific acoustic features found in vocalizations such as frequency modulations (Woolley and Casseday, 2005;Andoni et al, 2007), amplitude modulations (McAlpine, 2004;Woolley and Casseday, 2005), duration (Brand et al, 2000;Pérez-González et al, 2006), and/or combination sensitivity (Portfors and Wenstrup, 1999;Portfors, 2004).…”

Immunolocalization of vesicular glutamate transporters 1 and 2 in the rat inferior colliculus

“…VGLUT1 and VGLUT2 are both associated with glutamatergic terminals and their localizations are generally complementary without overlap (e.g. Hioki et al, 2003; The inferior colliculus (IC) receives multiple inputs from ascending and descending auditory pathways as well as from non-auditory inputs (Adams 1979, 1980, 1983, Aitkin et al, 1981Bajo and Moore, 2005;Cant & Benson, 2006;Jain & Shore, 2006;Loftus et al, 2004;Malmierca et al, 2005;Marsh et al, 2002;Merchan et al, 1994;Moore et al, 1998; Okayama et al, 2006;Oliver, 2000;Oliver et al, 1997; Osen, 1972;Saldana et al, 1996; Shofield, 2002; Shofield and Cant, 1996; Zhou, 2006, Tokunaga et al, 1984;Zhou and Shore, 2006) many of which are glutamatergic (Malmierca, 2003 for review;Alibardi, 1998;Feliciano and Potashner, 1995;Ross et al, 1995;Saint Marie, 1996, Suneja et al, 1995. The present study used co-immunolabeling to determine if VGLUT1 and VGLUT2 would differentiate unique and characteristic patterns of glutamatergic inputs onto neurons in the rat IC and to determine if there would be differences in the patterns in three sub-regions of the IC; the central nucleus (CIC), the lateral (external) cortex (LCIC) and the dorsal cortex (DCIC).…”