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Journal of Computational Neuroscience

Erschienen in:

06.10.2016

Optimal nonlinear cue integration for sound localization

verfasst von: Brian J. Fischer, Jose Luis Peña

Erschienen in: Journal of Computational Neuroscience | Ausgabe 1/2017

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Abstract

Integration of multiple sensory cues can improve performance in detection and estimation tasks. There is an open theoretical question of the conditions under which linear or nonlinear cue combination is Bayes-optimal. We demonstrate that a neural population decoded by a population vector requires nonlinear cue combination to approximate Bayesian inference. Specifically, if cues are conditionally independent, multiplicative cue combination is optimal for the population vector. The model was tested on neural and behavioral responses in the barn owl’s sound localization system where space-specific neurons owe their selectivity to multiplicative tuning to sound localization cues interaural phase (IPD) and level (ILD) differences. We found that IPD and ILD cues are approximately conditionally independent. As a result, the multiplicative combination selectivity to IPD and ILD of midbrain space-specific neurons permits a population vector to perform Bayesian cue combination. We further show that this model describes the owl’s localization behavior in azimuth and elevation. This work provides theoretical justification and experimental evidence supporting the optimality of nonlinear cue combination.

Vorheriger Artikel Artefactual origin of biphasic cortical spike-LFP correlation

Nächster Artikel Emergence of gamma motor activity in an artificial neural network model of the corticospinal system

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Alais, D., & Burr, D. (2004). The ventriloquist effect results from near-optimal bimodal integration. Current Biology, 14, 257–262.CrossRefPubMed

Albeck, Y., & Konishi, M. (1995). Responses of neurons in the auditory pathway of the barn owl to partially correlated binaural signals. Journal of Neurophysiology, 74, 1689–1700.PubMed

Angelaki, D. E., Gu, Y., & DeAngelis, G. C. (2009). Multisensory integration: psychophysics, neurophysiology, and computation. Current Opinion in Neurobiology, 19, 452–458.CrossRefPubMedPubMedCentral

Bala, A. D. S., Spitzer, M. W., & Takahashi, T. T. (2007). Auditory spatial acuity approximates the resolving power of space-specific neurons. PLoS ONE, 2, e675.CrossRefPubMedPubMedCentral

Battaglia, P. W., Jacobs, R. A., & Aslin, R. N. (2003). Bayesian integration of visual and auditory signals for spatial localization. Journal of the Optical Society of America A, 20, 1391–1397.CrossRef

Beck, J., Ma, W. J., Latham, P. E., & Pouget, A. (2007). Probabilistic population codes and the exponential family of distributions. Progress in Brain Research, 165, 509–519.CrossRefPubMed

Beck, J. M., Latham, P. E., & Pouget, A. (2011). Marginalization in neural circuits with divisive normalization. Journal of Neuroscience, 31, 15310–15319.CrossRefPubMedPubMedCentral

Brainard, M. S., & Knudsen, E. I. (1993). Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl. Journal of Neuroscience, 13, 4589–4608.PubMed

Brainard, M. S., Knudsen, E. I., & Esterly, S. D. (1992). Neural derivation of sound source location: resolution of spatial ambiguities in binaural cues. Journal of the Acoustical Society of America, 91, 1015–1027.CrossRefPubMed

Bregman AS (1994) Auditory scene analysis: The perceptual organization of sound. Cambridge, MA.: MIT press.

Carr, C. E., & Konishi, M. (1990). A circuit for detection of interaural time differences in the brain stem of the barn owl. Journal of Neuroscience, 10, 3227–3246.PubMed

Cazettes, F., Fischer, B. J., & Pena, J. L. (2014). Spatial cue reliability drives frequency tuning in the barn Owl’s midbrain. eLife, 3, e04854.CrossRefPubMedPubMedCentral

Cazettes, F., Fischer, B. J., & Peña, J. L. (2016). Cue reliability represented in the shape of tuning curves in the owl’s sound localization system. Journal of Neuroscience, 36, 2101–2110.CrossRefPubMedPubMedCentral

Christianson, G. B., & Peña, J. L. (2006). Noise reduction of coincidence detector output by the inferior colliculus of the barn owl. Journal of Neuroscience, 26, 5948–5954.CrossRefPubMedPubMedCentral

Cox, W., & Fischer, B. J. (2015). Optimal prediction of moving sound source direction in the owl. PLoS Computational Biology, 11, e1004360.CrossRefPubMedPubMedCentral

Edut, S., & Eilam, D. (2004). Protean behavior under barn-owl attack: voles alternate between freezing and fleeing and spiny mice flee in alternating patterns. Behavioural Brain Research, 155, 207–216.CrossRefPubMed

Egnor, R. S. (2001). Effects of binaural decorrelation on neural and behavioral processing of interaural level differences in the barn owl (Tyto alba). Journal of Comparative Physiology A, 187, 589–595.CrossRef

Eliasmith C., & Anderson C.H. (2004). Neural engineering: Computation, representation, and dynamics in neurobiological systems. Cambridge, MA: MIT Press.

Ernst, M. O., & Banks, M. S. (2002). Humans integrate visual and haptic information in a statistically optimal fashion. Nature, 415, 429–433.CrossRefPubMed

Fetsch, C. R., Pouget, A., DeAngelis, G. C., & Angelaki, D. E. (2011). Neural correlates of reliability-based cue weighting during multisensory integration. Nature Neuroscience, 15, 146–154.CrossRefPubMedPubMedCentral

Fischer, B. J., & Konishi, M. (2008). Variability reduction in interaural time difference tuning in the barn owl. Journal of Neurophysiology, 100, 708–715.CrossRefPubMedPubMedCentral

Fischer, B. J., & Peña, J. L. (2011). Owl’s behavior and neural representation predicted by Bayesian inference. Nature Neuroscience, 14, 1061–1066.CrossRefPubMedPubMedCentral

Fischer, B. J., Peña, J. L., & Konishi, M. (2007). Emergence of multiplicative auditory responses in the midbrain of the barn owl. Journal of Neurophysiology, 98, 1181–1193.CrossRefPubMedPubMedCentral

Fischer, B. J., Anderson, C. H., & Peña, J. L. (2009). Multiplicative auditory spatial receptive fields created by a hierarchy of population codes. PLoS One, 4, e8015.CrossRefPubMedPubMedCentral

Fux, M., & Eilam, D. (2009a). How barn owls (Tyto alba) visually follow moving voles (Microtus socialis) before attacking them. Physiology and Behavior, 98, 359–366.CrossRefPubMed

Fux, M., & Eilam, D. (2009b). The trigger for barn owl (Tyto alba) attack is the onset of stopping or progressing of the prey. Behavioural Processes, 81, 140–143.CrossRefPubMed

Girshick, A. R., Landy, M. S., & Simoncelli, E. P. (2011). Cardinal rules: visual orientation perception reflects knowledge of environmental statistics. Nature Neuroscience, 14, 926–932.CrossRefPubMedPubMedCentral

Gold, J. I., & Shadlen, M. N. (2001). Neural computations that underlie decisions about sensory stimuli. Trends in Cognitive Science, 5, 10–16.CrossRef

Gu, Y., Angelaki, D. E., & DeAngelis, G. C. (2008). Neural correlates of multisensory cue integration in macaque MSTd. Nature Neuroscience, 11, 1201–1210.CrossRefPubMedPubMedCentral

Hillis, J. M., Watt, S. J., Landy, M. S., & Banks, M. S. (2004). Slant from texture and disparity cues: optimal cue combination. Journal of Vision, 4, 1.CrossRef

Hollensteiner, K. J., Pieper, F., Engler, G., König, P., & Engel, A. K. (2015). Crossmodal integration improves sensory detection thresholds in the ferret. PLoS One, 10, e0124952.CrossRefPubMedPubMedCentral

Jacobs, R. A. (1999). Optimal integration of texture and motion cues to depth. Vision Research, 39, 3621–3629.CrossRefPubMed

Jazayeri, M., & Movshon, J. A. (2006). Optimal representation of sensory information by neural populations. Nature Neuroscience, 9, 690–696.CrossRefPubMed

Jeffress, L. A., Blodgett, H. C., & Deatherage, B. H. (1962). Effect of interaural correlation on the precision of centering a noise. Journal of the Acoustical Society of America, 34, 1122–1123.CrossRef

Johnson, D. H. (1980). The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. Journal of the Acoustical Society of America, 68, 1115–1122.CrossRefPubMed

Keller, C. H., Hartung, K., & Takahashi, T. T. (1998). Head-related transfer functions of the barn owl: measurement and neural responses. Hearing Research, 118, 13–34.CrossRefPubMed

Kita, H. & Armstrong, W. (1991). A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin. Journal of Neuroscience Methods, 37, 141–150.

Knill, D. C., & Pouget, A. (2004). The Bayesian brain: the role of uncertainty in neural coding and computation. Trends in Neurosciences, 27, 712–719.CrossRefPubMed

Knudsen, E. I. (1982). Auditory and visual maps of space in the optic tectum of the owl. Journal of Neuroscience, 2, 1177–1194.PubMed

Knudsen, E. I. (1983). Subdivisions of the inferior colliculus in the barn owl (Tyto alba). Journal of Comparative Neurology, 218, 174–186.CrossRefPubMed

Knudsen, E. I., & Konishi, M. (1978). A neural map of auditory space in the owl. Science, 200, 795–797.CrossRefPubMed

Knudsen, E. I., & Konishi, M. (1979). Mechanisms of sound localization in the barn owl (Tyto alba). Journal of Comparative Physiology, 133, 13–21.CrossRef

Knudsen, E. I., Konishi, M., & Pettigrew, J. D. (1977). Receptive fields of auditory neurons in the owl. Science, 198, 1278–1280.CrossRefPubMed

Knudsen, E. I., Blasdel, G. G., & Konishi, M. (1979). Sound localization by the barn owl (Tyto alba) measured with the search coil technique. Journal of Comparative Physiology, 133, 1–11.CrossRef

Koch, C. (2004). Biophysics of computation: information processing in single neurons. USA: Oxford University Press.

Konishi, M. (1993). Neuroethology of sound localization in the owl. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 173, 3–7.CrossRef

Köppl, C. (1997a). Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. Journal of Neuroscience, 17, 3312–3321.PubMed

Köppl, C. (1997b). Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. Journal of Neurophysiology, 77, 364–377.

Kullback, S., & Leibler, R. A. (1951). On information and sufficiency. Annals of Mathematical Statistics, 22, 79–86.CrossRef

Landy, M. S., & Kojima, H. (2001). Ideal cue combination for localizing texture-defined edges. Journal of the Optical Society of America A, 18, 2307.CrossRef

Landy, M. S., Maloney, L. T., Johnston, E. B., & Young, M. (1995). Measurement and modeling of depth cue combination: in defense of weak fusion. Vision Research, 35, 389–412.CrossRefPubMed

Landy MS, Banks MS, Knill DC (2011) Ideal-observer models of cue integration. Sensory Cue Integration: 5–29.

Ma, W. J., Beck, J. M., Latham, P. E., & Pouget, A. (2006). Bayesian inference with probabilistic population codes. Nature Neuroscience, 9, 1432–1438.CrossRefPubMed

Manley, G. A., Koppl, C., & Konishi, M. (1988). A neural map of interaural intensity differences in the brain stem of the barn owl. Journal of Neuroscience, 8, 2665–2676.PubMed

Middlebrooks, J. C., & Green, D. M. (1991). Sound localization by human listeners. Annual Review of Psychology, 42, 135–159.CrossRefPubMed

Mogdans, J., & Knudsen, E. I. (1994). Representation of interaural level difference in the VLVp, the first site of binaural comparison in the barn owl’s auditory system. Hearing Research, 74, 148–164.CrossRefPubMed

Moiseff, A. (1989). Bi-coordinate sound localization by the barn owl. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 164, 637–644.CrossRef

Moiseff, A., & Konishi, M. (1983). Binaural characteristics of units in the owl’s brainstem auditory pathway: precursors of restricted spatial receptive fields. Journal of Neuroscience, 3, 2553–2562.PubMed

Mysore, S. P., & Knudsen, E. I. (2012). Reciprocal inhibition of inhibition: a circuit motif for flexible categorization in stimulus selection. Neuron, 73, 193–205.CrossRefPubMedPubMedCentral

Mysore, S. P., & Knudsen, E. I. (2013). A shared inhibitory circuit for both exogenous and endogenous control of stimulus selection. Nature Neuroscience, 16, 473–478.CrossRefPubMedPubMedCentral

Niven, J. E., & Laughlin, S. B. (2008). Energy limitation as a selective pressure on the evolution of sensory systems. Journal of Experimental Biology, 211, 1792–1804.CrossRefPubMed

Nix, J., & Hohmann, V. (2006). Sound source localization in real sound fields based on empirical statistics of interaural parametersa). Journal of the Acoustical Society of America, 119, 463–479.CrossRefPubMed

Ohayon, S., van der Willigen, R. F., Wagner, H., Katsman, I., & Rivlin, E. (2006). On the barn owl’s visual pre-attack behavior: I. Structure of head movements and motion patterns. Journal of Comparative Physiology A, 192, 927–940.CrossRef

Ohshiro, T., Angelaki, D. E., & DeAngelis, G. C. (2011). A normalization model of multisensory integration. Nature Neuroscience, 14, 775–782.CrossRefPubMedPubMedCentral

Oruç, I., Maloney, L. T., & Landy, M. S. (2003). Weighted linear cue combination with possibly correlated error. Vision Research, 43, 2451–2468.CrossRefPubMed

Palmer, A. R., & Russell, I. J. (1986). Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells. Hearing Research, 24, 1–15.CrossRefPubMed

Pecka, M., Siveke, I., Grothe, B., & Lesica, N. A. (2010). Enhancement of ITD coding within the initial stages of the auditory pathway. Journal of Neurophysiology, 103, 38–46.CrossRefPubMed

Peña, J. L., & Konishi, M. (2000). Cellular mechanisms for resolving phase ambiguity in the owl’s inferior colliculus. Proceedings of the National Academy of Science, 97, 11787–11792.CrossRef

Peña, J. L., & Konishi, M. (2001). Auditory spatial receptive fields created by multiplication. Science, 292, 249–252.CrossRefPubMed

Peña, J. L., & Konishi, M. (2002). From postsynaptic potentials to spikes in the genesis of auditory spatial receptive fields. Journal of Neuroscience, 22, 5652–5658.PubMed

Peña, J. L., & Konishi, M. (2004). Robustness of multiplicative processes in auditory spatial tuning. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 24, 8907–8910.CrossRef

Roman, N., Wang, D., & Brown, G. J. (2003). Speech segregation based on sound localization. Journal of the Acoustical Society of America, 114, 2236–2252.CrossRefPubMed

Saberi, K., Takahashi, Y., Konishi, M., Albeck, Y., Arthur, B. J., & Farahbod, H. (1998). Effects of interaural decorrelation on neural and behavioral detection of spatial cues. Neuron, 21, 789–798.CrossRefPubMed

Shi, L., & Griffiths, T.L. (2009). Neural implementation of hierarchical Bayesian inference by importance sampling. In Y. Bengio, D. Schuurmans, J. Lafferty, C. Williams, & A. Culotta (Eds.), Advances in neural information processing systems 22 (pp. 1669–1677). Cambridge, MA: MIT Press.

Simoncelli, E.P. (2009). Optimal estimation in sensory systems. In M. Gazzaniga (Ed.), The cognitive neurosciences (vol. 4, pp. 525–535). Cambridge, MA: MIT Press.

Spitzer, M. W., Bala, A. D., & Takahashi, T. T. (2003). Auditory spatial discrimination by barn owls in simulated echoic conditions. Journal of the Acoustical Society of America, 113, 1631–1645.CrossRefPubMed

Stein, B. E., & Stanford, T. R. (2008). Multisensory integration: current issues from the perspective of the single neuron. Nature Review Neuroscience, 9, 255–266.CrossRef

Takahashi, T. T. (2010). How the owl tracks its prey–II. Journal of Experimental Biology, 213, 3399–3408.CrossRefPubMedPubMedCentral

Takahashi, T., Moiseff, A., & Konishi, M. (1984). Time and intensity cues are processed independently in the auditory system of the owl. Journal of Neuroscience, 4, 1781–1786.PubMed

van Beers, R. J., Sittig, A. C., & Gon, J. J. (1999). Integration of proprioceptive and visual position-information: an experimentally supported model. Journal of Neurophysiology, 81, 1355–1364.PubMed

Van Trees HL (2004) Detection, estimation, and modulation theory. New York, NY: Wiley.

Wagner, H., Takahashi, T., & Konishi, M. (1987). Representation of interaural time difference in the central nucleus of the barn owl’s inferior colliculus. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 7, 3105–3116.

Whitchurch, E. A., & Takahashi, T. T. (2006). Combined auditory and visual stimuli facilitate head saccades in the barn owl (Tyto alba). Journal of Neurophysiology, 96, 730–745.CrossRefPubMed

Wightman, F. L. & Kistler, D. J. (1993). Sound localization. In W. A. Yost, A. N. Popper, & R. R. Fay (Eds.), Human psychophysics (pp. 155–192). New York: Springer-Verlag.

Xu, J., Yu, L., Rowland, B. A., Stanford, T. R., & Stein, B. E. (2012). Incorporating cross-modal statistics in the development and maintenance of multisensory integration. Journal of Neuroscience, 32, 2287–2298.CrossRefPubMedPubMedCentral

Titel: Optimal nonlinear cue integration for sound localization
verfasst von: Brian J. Fischer
Jose Luis Peña
Publikationsdatum: 06.10.2016
Verlag: Springer US
Erschienen in: Journal of Computational Neuroscience / Ausgabe 1/2017
Print ISSN: 0929-5313
Elektronische ISSN: 1573-6873
DOI: https://doi.org/10.1007/s10827-016-0626-4

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