A novel relay nucleus between the inferior colliculus and the optic tectum in the chicken (Gallus gallus)

Abstract

Processing multimodal sensory information is vital for behaving animals in many contexts. The barn owl, an auditory specialist, is a classic model for studying multisensory integration. In the barn owl, spatial auditory information is conveyed to the optic tectum (TeO) by a direct projection from the external nucleus of the inferior colliculus (ICX). In contrast, evidence of an integration of visual and auditory information in auditory generalist avian species is completely lacking. In particular, it is not known whether in auditory generalist species the ICX projects to the TeO at all. Here we use various retrograde and anterograde tracing techniques both in vivo and in vitro, intracellular fillings of neurons in vitro, and whole-cell patch recordings to characterize the connectivity between ICX and TeO in the chicken. We found that there is a direct projection from ICX to the TeO in the chicken, although this is small and only to the deeper layers (layers 13-15) of the TeO. However, we found a relay area interposed among the IC, the TeO, and the isthmic complex that receives strong synaptic input from the ICX and projects broadly upon the intermediate and deep layers of the TeO. This area is an external portion of the formatio reticularis lateralis (FRLx). In addition to the projection to the TeO, cells in FRLx send, via collaterals, descending projections through tectopontine-tectoreticular pathways. This newly described connection from the inferior colliculus to the TeO provides a solid basis for visual-auditory integration in an auditory generalist bird. J. Comp. Neurol. 525:513-534, 2017. © 2016 Wiley Periodicals, Inc.

Heterogeneous organization and connectivity of the chicken auditory thalamus (Gallus gallus)

“…The owl ICx receives auditory inputs from the ICC and then provides spatial auditory information to the optic tectum (Knudsen and Knudsen, 1983). Recently, an indirect projection from an area overlapping with the location of E upon the optic tectum was identified in chickens, supporting the idea that E may participate in a similar function as the ICx in auditory-visual integration (Niederleitner and Luksch, 2012; Niederleitner et al, 2017). A difference between the two cell groups, though, is that the owl ICx does not contain projecting neurons to the thalamus as demonstrated by injections into the Ov complex (Proctor and Konishi, 1997), arguing that their comparison requires further investigation.…”

“Shepherd’s crook” neurons drive and synchronize the enhancing and suppressive mechanisms of the midbrain stimulus selection network

“…The peculiar bipolar morphology of Shc neurons would facilitate this integration, as their apical dendrites could summate visual inputs from different types of retinal ganglion cell terminals. The deep dendrites could add up auditory inputs arriving on deeper tectal layers (18,39) and also top-down influences from the arcopallium, which are able to bias the competing interactions within the isthmotectal system (31,40). The arcopallium can induce saccadic eye movements through a direct pathway to brainstem oculomotor centers and has been compared with the mammalian frontal eye fields (41); thus, Shcs may link stimulus selection to saccades, initiated by both pallial and mesencephalic circuits.…”

Expression patterns of ion channels and structural proteins in a multimodal cell type of the avian optic tectum

“…In chicken, the auditory signal is processed from the brainstem to two interconnected structures in the midbrain: the MLd and the TeO. The external part of the inferior colliculus (ICx) relays the auditory information either directly to the deeper layers of the optic tectum (Pena & Gutfreund, ) or across an external portion of the formatio reticularis lateralis (FRLx; Niederleitner, Gutierrez‐Ibanez, Krabichler, Weigel, & Luksch, ; Niederleitner & Luksch, ).…”

“…colliculus (ICx) relays the auditory information either directly to the deeper layers of the optic tectum (Pena & Gutfreund, 2014) or across an external portion of the formatio reticularis lateralis (FRLx; Niederleitner, Gutierrez-Ibanez, Krabichler, Weigel, & Luksch, 2017;Niederleitner & Luksch, 2012).…”