Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: A study using electron microscopic autoradiography

Abstract

The superior olivary complex is the first site in the central auditory system where binaural interactions occur. The output of these nuclei is direct to the central nucleus of the inferior colliculus, where binaural inputs synapse with monaural afferents such as those from the cochlear nuclei. Despite the importance of the olivary pathways for binaural information processing, little is known about their synaptic organization in the colliculus. The present study investigates the structure of the projections from the lateral and medial superior olivary nuclei to the inferior colliculus at the electron microscopic level. Stereotaxic placement and electrophysiological responses to binaural sounds were used to locate the superior olive. Anterograde axonal transport of 3H-leucine was combined with light and electron microscopic autoradiography to reveal the location and morphology of the olivary axonal endings. The results show that the superior olivary complex contributes different patterns of synaptic input to the central nucleus of the inferior colliculus. Each projection from the superior olivary complex to the colliculus differs in the number and combinations of endings. Axonal endings from the ipsilateral medial superior olive were exclusively the round (R) type that contain round synaptic vesicles and make asymmetrical synaptic junctions. This morphology is usually associated with excitatory synapses and neurotransmitters such as glutamate. Endings from medial superior olive terminate densely in the central nucleus. The projection from the contralateral lateral superior olive also terminates primarily as R endings. This projection also includes small numbers of pleomorphic (PL) endings that contain pleomorphic synaptic vesicles and usually make symmetrical synaptic junctions. The PL morphology is associated with inhibitory synapses and transmitters such as gamma-aminobutyric acid and glycine. All endings from the contralateral lateral superior olive terminate much less densely than endings from the medial olive. In contrast, the projection from the ipsilateral lateral superior olive contributes both R and PL endings in roughly equal proportions. These ipsilateral afferents are heterogeneous in density and can terminate in lower or higher concentrations than endings from the contralateral side. These data show that the superior olive is a major contributor to the synaptic organization of the central nucleus of the inferior colliculus. The ipsilateral projections of the medial and lateral superior olive may produce higher concentrations of R endings than other inputs to the central nucleus. Such endings may participate in excitatory synapses. The highest concentrations of PL endings come from the ipsilateral lateral superior olive.(ABSTRACT TRUNCATED AT 400 WORDS)

Duration Tuning across Vertebrates

“…Neurons with transient, onset-evoked responses are found throughout the central auditory pathway, including the cochlear nucleus (Pfeiffer, 1966;Haplea et al, 1994) and (medial) superior olive (Guinan et al, 1972;Grothe et al, 1997Grothe et al, , 2001. Offset responding neurons have also been observed in the (medial) superior olivary complex (Guinan et al, 1972;Grothe et al, 1997Grothe et al, , 2001, where dense excitatory projections lead into the ICc (Oliver et al, 1995). GABAergic offset responding neurons in the superior paraolivary complex are not candidates for providing offset-evoked excitatory input to the inferior colliculus (IC) but may still contribute to duration tuning by suppressing excitatory offset responses at some durations (Kadner et al, 2006).…”

Electrical Stimulation of the Midbrain for Hearing Restoration: Insight into the Functional Organization of the Human Central Auditory System

“…The findings for AMI-2 further suggest that a segregated group (or at least a predominance) of ipsilaterally excited projections to the IC exist within the ventral portion of the lateral lemniscus in humans. Considering that the medial olivary nucleus is enlarged whereas the lateral olivary nucleus is reduced in humans compared with animals (Moore, 1987) and only a small proportion of ipsilaterally excited pathways to the IC appear to originate from the cochlear nucleus and periolivary region, this segregated region may correspond predominantly to fibers from the medial superior olive (Nordeen et al, 1983;Oliver, 1987;Masterton et al, 1992;Oliver et al, 1995;Schofield, 2005). This is interesting in that projections from the brainstem nuclei to the IC tend to be more excited contralaterally based on animal studies, yet stimulation of an ϳ2 mm midbrain region elicited only ipsilateral percepts.…”

Neuronal Responses to Lemniscal Stimulation in Laminar Brain Slices of the Inferior Colliculus

“…In the present study, the slice plane allows more of the dendritic tree to remain intact, and the lemniscal fibers that course parallel to the lamina/dendrites also remain intact. This may preserve the multiple, en passant, axodendritic synapses from lemniscal axons that terminate on ICC neurons (Oliver et al 1995;Oliver et al 1999). Consequently, the stimulation of a single lemniscal axon may be more effective because more of its inputs to a single neuron may be preserved.…”