The neuronal architecture of the inferior colliculus in the cat: Defining the functional anatomy of the auditory midbrain

Abstract

This study defines anatomical subdivisions in Golgi-impregnated material from the inferior colliculus of the cat. The findings demonstrate that the inferior colliculus consists of a mosaic of morphologically distinct parts of neuropil. Each part is also characterized by a unique set of neuronal types. Each part of the inferior colliculus can be defined as tectal or tegmental on the basis of the fundamental pattern of dendritic branching. The main subdivisions of the auditory tectum are the central nucleus, the cortex, and the paracentral nuclei. The central nucleus is distinguished by its laminated neuropil composed of neurons with disc-shaped dendritic fields oriented in parallel arrays with the lemniscal axons. In contrast, the cortex is identified by its broad layers of loosely woven neuropil, which are orthogonal to those in the central nucleus and lack neurons with disc-shaped dendritic fields. The paracentral nuclei, so called because of their scattered arrangement around the central nucleus, are the commissural, dorsomedial, rostral pole, lateral, and ventrolateral nuclei. The main subdivisions of the auditory tegmentum are the pericollicular areas, the nucleus of the brachium of the inferior colliculus, and the sagulum. The pericollicular areas are intercollicular or subcollicular and separate the tectal division from the superior colliculus, central gray, and remaining portions of the tegmentum. The afferent projections to each tectal and tegmental subdivision, as observed in silver-degeneration experiments, distinguish the parcellations based on the Golgi findings. Subdivisions containing tectal cell types receive afferents predominantly from the auditory pathways, in contrast to subdivisions with tegmental cell types, which receive inputs from a wide variety of sources. This suggests a correlation between neuronal types and the nature of their inputs. This analysis of the subdivisions of the inferior colliculus differs from previous studies, especially those relying on Nissl stains. It is likely that subdivisions distinguished by the pattern of the neuropil differ functionally, since the structural components identified in the Golgi-impregnated material are essential parts of the synaptic organization of the auditory midbrain. Future physiological studies should benefit from approaches in which the cell types serve as the focus for the analysis.

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

“…Neurons in the IC were differentiated based on size (Faye-Lund and Osen, 1985; Malmierca et al, 1993Malmierca et al, , 1995Morest & Oliver, 1984; Oliver refs. Peruzzi et al, 2000).…”

Quantitative assessment of developing afferent patterns in the cat inferior colliculus revealed with calbindin immunohistochemistry and tract tracing methods

“…Morest and Oliver (1984) described the cat IC as comprising tectal and tegmental regions based on rapid Golgi staining of cells and axons. The tectal component they described consisted of a large, CNIC characterized by its predominant disk-shaped cells, a cortex (both dorsal and caudal to the CNIC), and various paracentral nuclei.…”

“…In the auditory midbrain, the inferior colliculus (IC) is comprised of a large, seemingly homogeneous, central nucleus (CNIC) surrounded by a complex and heterogeneous arrangement of several paracentral nuclei (Berman, 1968;Rockel and Jones, 1973a,b;Morest and Oliver, 1984 (Rockel and Jones, 1973a;Oliver and Morest, 1984). With only a few exceptions, all ascending hindbrain auditory pathways project to the CNIC and end in cochleotopic fashion within a series of these fibrodendritic layers.…”

“…The results reveal a neurochemical marker for one type of synaptic compartment in CNIC layers, banding, that is organized before hearing onset in kittens, but that may undergo some postnatal pruning. Keywords fibrodendritic laminae; banding pattern; calcium-binding proteins; lateral superior olivary nucleus; carbocyanine dyeIn the auditory midbrain, the inferior colliculus (IC) is comprised of a large, seemingly homogeneous, central nucleus (CNIC) surrounded by a complex and heterogeneous arrangement of several paracentral nuclei (Berman, 1968;Rockel and Jones, 1973a,b;Morest and Oliver, 1984 (Rockel and Jones, 1973a;Oliver and Morest, 1984). With only a few exceptions, all ascending hindbrain auditory pathways project to the CNIC and end in cochleotopic fashion within a series of these fibrodendritic layers.…”

Identification of cell types in brain slices of the inferior colliculus

“…In the cat, disc-shaped neurons have dendrites oriented in parallel to create ®bro-dendritic laminae, while stellate neurons are perpendicular to the laminae. 26,32,33,51,52 In the rat, the thickness of the dendritic tree, rather than the orientation is more diagnostic. Two neuron classes (¯at and less-¯at) are seen in adult rats, but both types parallel the laminae.…”