Descending projections to the auditory midbrain: evolutionary considerations

Abstract

The mammalian inferior colliculus (IC) is massively innervated by multiple descending projection systems. In addition to a large projection from the auditory cortex (AC) primarily targeting the non-lemniscal portions of the IC, there are less well-characterized projections from non-auditory regions of the cortex, amygdala, posterior thalamus and the brachium of the IC. By comparison, the frog auditory midbrain, known as the torus semicircularis, is a large auditory integration center that also receives descending input, but primarily from the posterior thalamus and without a projection from a putative cortical homolog: the dorsal pallium. Although descending projections have been implicated in many types of behaviors, a unified understanding of their function has not yet emerged. Here, we take a comparative approach to understanding the various top-down modulators of the IC to gain insights into their functions. One key question that we identify is whether thalamotectal projections in mammals and amphibians are homologous and whether they interact with evolutionarily more newly derived projections from the cerebral cortex. We also consider the behavioral significance of these descending pathways, given anurans' ability to navigate complex acoustic landscapes without the benefit of a corticocollicular projection. Finally, we suggest experimental approaches to answer these questions.

Keywords: Anuran; Auditory cortex; Bat; Corticofugal; Echolocation; Frog; Inferior colliculus; Thalamus.

Fig. 1:

Diagrams of the major structures and connections in the anuran and mammalian central auditory systems. Where projections are bilateral, only the stronger of the two is drawn, for purposes of clarity. AC = auditory cortex, AMY = amygdala, AP = amphibian papilla, BP = basilar papilla, DMN = dorsomedial nucleus, IC = inferior colliculus (C=central nucleus, D=dorsal cortex, L=lateral cortex), MGB = medial geniculate body (D=dorsal, V=ventral, M=medial), NLL = nuclei of lateral lemniscus (V=ventral, D=dorsal), SON = superior olivary nuclei (LSO = lateral superior olive, MSO=medial superior olive, MNTB = medial nucleus of the trapezoid body), STR = striatum, THAL = thalamus (C=caudal, P=posterior). TS = torus semicircularis (P=principal, L=laminar, M=magnocellular).

Fig. 2:

The impact of thalamic stimulation on midbrain responses to fictive acoustic stimulation in the frog. A) Top: location of stimulating electrode in the thalamus, Bottom: location of the stimulating electrode in the eighth nerve. B) Top: Impact of electrical stimulation of eighth nerve on spiking in a midbrain neuron, recorded intracellularly. Arrowhead = stimulus artifact. Middle: Impact of stimulation of the thalamus, showing a hyperpolarizing response after an initial spike. Bottom: simultaneous stimulation of eighth nerve and thalamus, showing a diminished number of spikes compared to eighth nerve stimulation alone. C) Summary data in terms of action potentials (APs, top, n=5 cells) or post-synaptic potentials (PSPs, bottom, n=6 cells) in response to combined bottom-up and top-down stimulation. Figures from Endepols and Walkowiak 2001, with permission.

Fig. 3:

Diagrammatic representations of the potential relationships between corticocollicular projections and evolutionarily-ancient thalamotectal projections. Left: A fully integrated model whereby corticothalamic axons activate thalamotectal neurons via a branch of a corticocollicular axon. Both systems synapse on and influence the same neuron in the colliculus. Right: A fully segregated model whereby thalamotectal and corticocollicular projections do not converge on any common targets.

Fig. 4:

Albert Feng in his laboratory, in the late 1970’s (courtesy of the Feng Family).