Tracking moving acoustic targets in complex natural scenes is crucial for communication and survival. Sound-motion sensitivity requires the ability to detect time-dependent changes in sounds. This function is especially pertinent to a predator species such as the barn owl, which must track and predict the position of moving prey. Barn owls hunt successfully in total darkness using only auditory cues. They exhibit a map of auditory space in the external nucleus of the inferior colliculus (ICx), the circuit and computation of which has been elucidated to an extent that makes this species a powerful system to study the neural coding of auditory space. However, the mechanisms of achieving motion-direction selectivity and mapping auditory motion have been poorly studied in the auditory system. Auditory spatial receptive fields (RFs) have traditionally been approached as invariant response properties and only few studies have addressed how spatial tuning changes in time. As demonstrated in the visual system, spatial RFs are better characterized in a joint space-time domain, as the shape and polarity of RFs'sub regions may change over the course of the response. In this study, we will investigate the properties and circuitry of spatiotemporal RFs in the ICx and their predictive power for sound-motion selectivity. Our preliminary results show asymmetries in RFs on the single-cell and population level that are consistent with motion-direction selectivity. We hypothesize that these RF properties are mediated by asymmetric lateral inhibition and enable a preference for sound-direction selectivity across the entire population of ICx neurons.
In Aim 1, we will investigate RF spatiotemporal properties using spatial white-noise stimuli. We will use reverse correlation methods to construct the time-dependent structure of spatial RFs and interactions with neighboring areas of the map. Our preliminary data suggests that surround inhibition is non-symmetric, thus providing a basis for sound-motion direction selectivity. We will test this hypothesis by comparing RF dynamics and direction-selectivity measured with real sound motion and testing local inhibitory networks by iontophoresis of inhibitory transmitter blockers.
In Aim 2, we will study the spatiotemporal RFs over the left and right ICx and investigate the population mechanisms through modeling and physiology. We will design a network model using known ICx topographic organization and RF properties to test if the observed bias can be caused by structural asymmetry in bilateral inhibitory input and test predictions of this model. Finally, we will study the behavioral role of the population bias in direction selectivity in Aim 3 using psychoacoustics. The proposed study is the first instance white-noise analysis in real space is performed in the auditory system and the first time any spatial white-noise analysis is conducted in a topographic representation of auditory space.

Public Health Relevance

The proposed research investigates how the brain locates and tracks moving sounds in space by testing hypotheses based on human and animal models. How the brain represents acoustic motion is an outstanding open question in the field. Elucidating this question can help to understand and treat patients inflicted by diseases of the auditory system as well as to engineer and improve neural prosthetic devices that can restore or enhance hearing.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
Predoctoral Individual National Research Service Award (F31)
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Special Emphasis Panel (ZDC1-SRB-L (45))
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Sklare, Dan
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Albert Einstein College of Medicine
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Wang, Yunyan; Peña, José Luis (2013) Direction selectivity mediated by adaptation in the owl's inferior colliculus. J Neurosci 33:19167-75
Wang, Yunyan; Shanbhag, Sharad J; Fischer, Brian J et al. (2012) Population-wide bias of surround suppression in auditory spatial receptive fields of the owl's midbrain. J Neurosci 32:10470-8