Capturing nature's statistical structure in the neural coding is essential for optimal adaptation to the environment. This proposal investigates this issue by asking how the brain can approach statistical optimality in the sound localization system of barn owls. A Bayesian theoretical framework will be used to describe how sensory and a priori information can be combined optimally to guide orienting behavior. Specifically, we seek to demonstrate that sensory reliability and a priori information are represented in the response properties and topography of the neural population that represents auditory space.
The first aim studies how sensory cue reliability is represented in the brain. Optimal use of sensory information requires that the statistical reliability of sensory cues is accessible from neural responses. Previous theories have suggested that cue reliability is encoded in the gain of neural responses or alternatively the selectivity of neural responses but how reliability is represented is not known. In the owl, changes in the statistical reliability of spatial cues resultin changes in sound localization behavior consistent with a Bayesian model. Our model predicts that the reliability is encoded in the tuning curve widths of space-specific neurons located in the owl's midbrain. We will manipulate tuning-curve widths and firing rates independently to test this hypothesis and test the model with behavior.
The second aim will study whether the integration of spatial cues for sound localization follows the rules of statistical optimality. Perception in natural environments often depends on the integration of multiple cues, both within modalities and across modalities. Here, whether the integration is linear or nonlinear is crucial, as extending a Bayesian model from one to two dimensions indicates that optimal combination of conditionally independent sensory cues should be nonlinear. In the owl's brain, the spatial cues used to determine elevation and azimuth are processed independently and combined nonlinearly in the midbrain to form spatial receptive fields. However, whether or not sound localization cues are conditionally independent is unknown.
This aim will demonstrate why nonlinear operations are essential for optimal cue combination and how they arise. We will perform in vivo intracellular recording and behavioral tests to address these questions. This will provide an experimental test of the prediction that optimal combination of conditionally independent cues is nonlinear.
The third aim will extend the model to coding dynamic auditory scenes;the time dimension will be incorporated into the Bayesian model of sound localization. We will use a population vector model to determine how a neural system can achieve predictive power in auditory space through Bayesian inference. We will measure receptive fields of midbrain neurons in space and time to test the hypothesis that the owl has a bias for sources moving toward the center of gaze. We will use behavioral tests to measure detection thresholds for moving sound sources. Finally, we will study whether a dynamic gain control in a non-uniform network can account for Bayesian predictive coding of sound motion with a bias for sources moving toward the center of gaze. Broader Impacts: Outstanding open questions of how statistics of natural scenes are captured by neural coding include how reliability of sensory information is represented and combined with prior probabilistic knowledge, and how sensory cues are integrated to optimally guide behavior. This project addresses these questions in the heterogeneous representation of space of the owl's auditory midbrain. Whether non-uniform representations can be decoded using a population vector to perform Bayesian inference and that this mechanism works in multiple dimensions transcends sound localization in barn owls, becoming of general interest to neural coding. The PIs involved in this project, one of them a junior researcher, gather complementary expertise in modeling, physiology and behavioral approaches allowing for a truly interdisciplinary approach. This project will thus consolidate a powerful collaboration while providing groundbreaking information on outstanding questions in Neuroscience. The three institutions involved are committed to the training of underrepresented groups. The location of the Albert Einstein College of Medicine in the Bronx, makes it a pole of development in one of the most diverse and poor counties in the country and provides the potential for direct access to translational research. The inclusion of the Department of Mathematics at Seattle University, ranked among the top ten universities in the West for undergraduate programs, and the University of Oregon will ensure that this project will enhance training from the undergraduate to postdoctoral levels.
|Cazettes, Fanny; Fischer, Brian J; Beckert, Michael V et al. (2018) Emergence of an Adaptive Command for Orienting Behavior in Premotor Brainstem Neurons of Barn Owls. J Neurosci 38:7270-7279|
|Fischer, Brian J; Peña, Jose Luis (2017) Optimal nonlinear cue integration for sound localization. J Comput Neurosci 42:37-52|
|Carr, Catherine E; Peña, Jose L (2016) Cracking an improbable sensory map. J Exp Biol 219:3829-3831|
|Cazettes, Fanny; Fischer, Brian J; Peña, Jose L (2016) Cue Reliability Represented in the Shape of Tuning Curves in the Owl's Sound Localization System. J Neurosci 36:2101-10|
|Keller, Clifford H; Takahashi, Terry T (2015) Spike timing precision changes with spike rate adaptation in the owl's auditory space map. J Neurophysiol 114:2204-19|
|Cox, Weston; Fischer, Brian J (2015) Optimal Prediction of Moving Sound Source Direction in the Owl. PLoS Comput Biol 11:e1004360|
|Rich, Dylan; Cazettes, Fanny; Wang, Yunyan et al. (2015) Neural representation of probabilities for Bayesian inference. J Comput Neurosci 38:315-23|
|Cazettes, Fanny; Fischer, Brian J; Pena, Jose L (2014) Spatial cue reliability drives frequency tuning in the barn Owl's midbrain. Elife 3:e04854|
|Pena, Jose L; Gutfreund, Yoram (2014) New perspectives on the owl's map of auditory space. Curr Opin Neurobiol 24:55-62|
|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|