A Candidate Pathway for a Visual Instructional Signal to the Barn Owl's Auditory System

Abstract

Many organisms use multimodal maps to generate coherent neuronal representations that allow adequate responses to stimuli that excite several sensory modalities. During ontogeny of these maps, one modality typically acts as the dominant system the other modalities are aligned to. A well studied model for the alignment of sensory maps is the calibration of the auditory space map by the visual system in the optic tectum of the barn owl. However, a projection from the optic tectum to the site of plasticity in the auditory pathway that could deliver an instructive signal has not been found so far. We have analyzed the development of the connectivity between the bimodal (visual and auditory) map of space in the barn owl's optic tectum and the auditory space map in the inferior colliculus with tracing methods and intracellular fills. Neurons in the tectal stratum griseum centrale were found to be suited to deliver an alignment signal from the visual midbrain to the auditory pathway. These neurons are presumably part of the efferent tectal projection pathway that mediates head saccades. The implications of a sensory alignment signal possibly being delivered by a (pre)motor command pathway are discussed.

Sounds, signals and space maps

“…But they would have different neural substrates: a global value signal would require a diffuse projection to the auditory space map; and a spatial template would require a point-to-point projection. So the earlier results 6,7 support the idea of a spatial template.…”

Stimulus-Specific Adaptation: Can It Be a Neural Correlate of Behavioral Habituation?

“…However, this interpretation is complicated by the fact that there are multiple loops. The OT projects back to the ICX (Hyde and Knudsen, 2000;Luksch et al, 2000;Gutfreund et al, 2002). The E is likely to form a loop with the optic tectum through the auditory arcopallium (Knudsen et al, 1995;Shimizu and Bowers, 1999), which also sends projections to the ICX (Knudsen et al, 1995).…”

Rapid Adaptation to Auditory-Visual Spatial Disparity

“…In the inferior colliculus, auditory information is integrated to create topographically organized maps of both frequency and space, formed by neurons exhibiting relatively sharp-frequency tuning and spatial selectivity (Semple et al 1983;Aitkin et al 1984Aitkin et al , 1985Moore et al 1984a,b;for review, see Konishi 1986). In the barn owl, the topographical representation of auditory space in the external subnucleus of the inferior colliculus homolog has been shown to be calibrated by a visual instructional signal, originating in the visual map of the optic tectum, which arises from topographic projections from the retina Knudsen 1993, 1995;Feldman and Knudsen 1997;Hyde andKnudsen 2000, 2002;Knudsen et al 2000;Luksch et al 2000;DeBello et al 2001;Zheng and Knudsen 2001). Investigations in mammals have been far less extensive, but mechanisms similar to those in the owl may occur (King 1993;King et al 2000).…”

“…However, there is evidence from experiments on owls, reared with prismatic spectacles, that both midbrain representations of auditory space and sound localization behaviour are shifted in the direction of visual displacement (Knudsen andKnudsen 1985, 1989;Brainard and Knudsen 1993;Knudsen 1999;Hyde andKnudsen 2000, 2002;Zheng and Knudsen 2001). These processes may rely on neural mechanisms on the basis of simple Hebbian learning rules (Feldman et al 1996;Knudsen et al 2000;Luksch et al 2000). Even though these animal studies refer to longlasting reorganizations, partially restricted to specific sensitive periods in development (Brainard and Knudsen 1995;Feldman and Knudsen 1997;DeBello et al 2001; for review, see Sur et al 1990), the concept that vision calibrates sound localization may also apply to potentially rapidly induced neural plasticity in the human cortex.…”