Neural Maps of Interaural Time Difference in the American Alligator: A Stable Feature in Modern Archosaurs

Abstract

Detection of interaural time differences (ITDs) is crucial for sound localization in most vertebrates. The current view is that optimal computational strategies of ITD detection depend mainly on head size and available frequencies, although evolutionary history should also be taken into consideration. In archosaurs, which include birds and crocodiles, the brainstem nucleus laminaris (NL) developed into the critical structure for ITD detection. In birds, ITDs are mapped in an orderly array or place code, whereas in the mammalian medial superior olive, the analog of NL, maps are not found. As yet, in crocodilians, topographical representations have not been identified. However, nontopographic representations of ITD cannot be excluded due to different anatomical and ethological features of birds and crocodiles. Therefore, we measured ITD-dependent responses in the NL of anesthetized American alligators of either sex and identified the location of the recording sites by lesions made after recording. The measured extracellular field potentials, or neurophonics, were strongly ITD tuned, and their preferred ITDs correlated with the position in NL. As in birds, delay lines, which compensate for external time differences, formed maps of ITD. The broad distributions of best ITDs within narrow frequency bands were not consistent with an optimal coding model. We conclude that the available acoustic cues and the architecture of the acoustic system in early archosaurs led to a stable and similar organization in today's birds and crocodiles, although physical features, such as internally coupled ears, head size, or shape, and audible frequency range, vary among the two groups.

Synthesis of Hemispheric ITD Tuning from the Readout of a Neural Map: Commonalities of Proposed Coding Schemes in Birds and Mammals

“…Seminal work by Harper and McAlpine (2004) provided an explanation of how topographic ITD representations could maximize information, based on the species' head size and frequency range over which ITD is encoded. Although this theory may not apply to all species (Kettler and Carr, 2019), it does for barn owls, given their physiological range of ITD and the unusually broad frequency range over which their brain can encode ITD (Carr and Konishi, 1990;Köppl, 1997). Recent findings showing that this space map is also a frequency map that excludes frequency ranges carrying unreliable spatial information (Cazettes et al, 2014) and can represent sensory reliability (Cazettes et al, 2016) further illuminate the evolutionary advantage of this specialization.…”

“…In both birds and mammals, the timing of acoustic signals is sensed by receptor cells of the cochlea and transmitted to the cochlear nuclei through the auditory nerve fibers. ITD is first detected by coincidence detector neurons receiving bilateral projections from the cochlear nuclei, located in the nucleus laminaris in birds and alligators (Carr and Konishi, 1990;Köppl and Carr, 2008;Kettler and Carr, 2019) and the medial superior olive (MSO) in mammals (Goldberg and Brown, 1969;Yin and Chan, 1990;Spitzer and Semple, 1995). Information about ITD is conveyed to the inferior colliculus (IC) across vertebrate species.…”

The anatomical basis of amphibious hearing in the American alligator (Alligator mississippiensis)

“…The majority of tympanic vertebrates, and all known reptiles, localize sounds using bilateral temporal cues (e.g., Oertel, 1999; Winer & Schreiner, 2005). These bilateral temporal signals are converted into spatial cues using a variety of neural computational systems; the spatial cues, in turn, form an acoustic map of the animal's environment (e.g., Christensen‐Dalsgaard & Carr, 2018; Kettler & Carr, 2019). Although this auditory localization system has been extensively studied in a variety of vertebrates (Walton et al, 2017), one aspect remains poorly understood.…”

Differences in the neural representation of binaural sound localization cues in the auditory midbrain of chicken and barn owl

“…In the barn owl, IC subregions can be readily distinguished by anatomical features, as well as through the different selectivities of their neurones for frequency and for sound-localization cues. In the barn owl IC, the separate brainstem processing streams for the two principal binaural cues, interaural time (ITD) and interaural level (ILD) difference, terminate and subsequently converge for the first time, ultimately generating a two-dimensional neural representation of auditory space (reviewed by, e.g., Kettler & Carr, 2019; Konishi, 2003; Singheiser et al, 2012).…”