Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey

Abstract

Projections from the posterior thalamus and medial geniculate body were labeled retrogradely with wheat germ agglutinin conjugated to horseradish peroxidase injected into the rat, cat, and squirrel monkey inferior colliculus. Neurons were found ipsilaterally in the (1) medial division of the medial geniculate body, (2) central gray, (3) posterior limitans nucleus, and the (4) reticular part of the substantia nigra. Bilateral projections involved the (5) peripeduncular/suprapeduncular nucleus, (6) subparafascicular and posterior intralaminar nuclei, (7) nucleus of the brachium of the inferior colliculus, (8) lateral tegmental/lateral mesencephalic areas, and (9) deep layers of the superior colliculus. The medial geniculate projection was concentrated in the caudal one-third of the thalamus; in contrast, the labeling in the subparafascicular nucleus, substantia nigra, and central gray continued much further rostrally. Robust anterograde labeling corresponded to known patterns of tectothalamic projection. Biotinylated dextran amine deposits in the rat inferior colliculus revealed that (1) many thalamotectal cells were elongated multipolar neurons with long, sparsely branched dendrites, resembling neurons in the posterior intralaminar system, and that other labeled cells were more typical of thalamic relay neurons; (2) some cells have reciprocal projections. Similar results were seen in the cat and squirrel monkey. The widespread origins of descending thalamic influences on the inferior colliculus may represent a phylogenetically ancient feedback system onto the acoustic tectum, one that predates the corticocollicular system and modulates nonauditory centers and brainstem autonomic nuclei. Besides their role in normal hearing such pathways may influence behaviors ranging from the startle reflex to the genesis of sound-induced seizures.

Introduction

The inferior colliculus is a critical part of the ascending auditory system, and it is essential for normal hearing (Aitkin, 1986) and for accurate spatial orientation to sound (Jane et al., 1965). It receives afferent input from several medullary and pontine auditory nuclei (Beyerl, 1978). Its main upstream target is the medial geniculate body (LeDoux et al., 1987) and, to a lesser extent, the superior colliculus (Frisina et al., 1989). Classically, the thalamus has been seen as essentially a part of the ascending projection system, with little descending or reciprocal input to prethalamic nuclei (Schwartz, 1992). The primary descending projection instead arises in the auditory cortex (Andersen et al., 1980, Aitkin, 1986, Winer et al., 1998a). The absence of such reciprocal projections between the thalamus and the midbrain would seem to set the medial geniculate body apart since many collicular and subcollicular nuclei have descending interconnections with one another (Huffman and Henson, 1990). However, reports in several species find that the inferior colliculus receives modest descending input from various thalamic and perithalamic tegmental nuclei (Adams, 1980, Yasui et al., 1992, Frisina et al., 1997) and recent studies in the gerbil have documented the descending projections of single thalamic cells in tissue slices (Kuwabara and Zook, 2000). Estimates of the complete origin of such projections require sensitive retrograde tracers injected in the inferior colliculus. A second issue is the identity of morphological subtypes of thalamotectal neurons. This is pertinent to understanding the nature of the information that they might transmit to the midbrain. It is also unknown whether thalamotectal cells themselves receive ascending input from the inferior colliculus. If they operate independently, then their major synaptic influence may be cortical. Finally, it remains to establish whether the thalamotectal projection is similar in different mammals. Here, we report that these connections are more widespread and somewhat larger than expected, that they are concentrated in both sensory and intralaminar thalamic nuclei, that they involve different types of thalamotectal neurons in the sensory and posterior intralaminar systems, that some thalamotectal neurons are targets of complementary tectothalamic projections, and that this pathway has a similar organization in rodent, carnivore, and primate species. These features suggest that the descending thalamofugal system may have roles in auditory processing and extraauditory function that remain to be discerned.