New perspectives on the owl's map of auditory space

A map of sound direction was found in the owl's midbrain more than three decades ago. This finding suggested that the brain reconstructs spatial coordinates to represent them. Subsequent research elucidated the variables used to compute the map. Here we provide a review of the processes leading to its emergence and an updated perspective on how and what information is represented.

[1]  E I Knudsen,et al.  A neural map of auditory space in the owl. , 1978, Science.

[2]  T T Takahashi,et al.  Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl , 1988, The Journal of comparative neurology.

[3]  E I Knudsen,et al.  Adaptive Axonal Remodeling in the Midbrain Auditory Space Map , 2001, The Journal of Neuroscience.

[4]  Brian J. White,et al.  Microstimulation of the Monkey Superior Colliculus Induces Pupil Dilation Without Evoking Saccades , 2012, The Journal of Neuroscience.

[5]  E. Knudsen,et al.  Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  E I Knudsen,et al.  Neural derivation of sound source location: resolution of spatial ambiguities in binaural cues. , 1992, The Journal of the Acoustical Society of America.

[7]  M. Spezio,et al.  Frequency-Specific Interaural Level Difference Tuning Predicts Spatial Response Patterns of Space-Specific Neurons in the Barn Owl Inferior Colliculus , 2003, The Journal of Neuroscience.

[8]  Klaus Hartung,et al.  Representation of sound source direction in the superior colliculus of the guinea pig in a virtual auditory environment , 2002, Experimental Brain Research.

[9]  Y. Gutfreund,et al.  Stimulus-Specific Adaptations in the Gaze Control System of the Barn Owl , 2008, The Journal of Neuroscience.

[10]  Terrence R Stanford,et al.  Alterations to multisensory and unisensory integration by stimulus competition. , 2011, Journal of neurophysiology.

[11]  E I Knudsen,et al.  Topographic projection from the optic tectum to the auditory space map in the inferior colliculus of the barn owl , 2000, The Journal of comparative neurology.

[12]  G. Freyd,et al.  Separate Signals for Target Selection and Movement Specification in the Superior Colliculus , 2022 .

[13]  M Konishi,et al.  Auditory Spatial Receptive Fields Created by Multiplication , 2001, Science.

[14]  T. Takahashi,et al.  An anatomical substrate for the inhibitory gradient in the VLVp of the owl , 1995, The Journal of comparative neurology.

[15]  Terry T. Takahashi,et al.  Prediction of auditory spatial acuity from neural images on the owl's auditory space map , 2003, Nature.

[16]  Richard J Krauzlis,et al.  Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments , 2010, Nature Neuroscience.

[17]  E I Knudsen,et al.  Neural maps of head movement vector and speed in the optic tectum of the barn owl. , 1990, Journal of neurophysiology.

[18]  Israel Nelken,et al.  Sound-Localization Experiments with Barn Owls in Virtual Space: Influence of Interaural Time Difference on Head-Turning Behavior , 2000, Journal of the Association for Research in Otolaryngology.

[19]  Haim Sompolinsky,et al.  A Hebbian learning rule mediates asymmetric plasticity in aligning sensory representations. , 2008, Journal of neurophysiology.

[20]  Hermann Wagner,et al.  Distribution of Interaural Time Difference in the Barn Owl's Inferior Colliculus in the Low- and High-Frequency Ranges , 2007, The Journal of Neuroscience.

[21]  M Konishi,et al.  A neural map of interaural intensity differences in the brain stem of the barn owl , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  Shreesh P Mysore,et al.  Flexible Categorization of Relative Stimulus Strength by the Optic Tectum , 2011, The Journal of Neuroscience.

[23]  E I Knudsen,et al.  Computational maps in the brain. , 1987, Annual review of neuroscience.

[24]  M. Konishi,et al.  Projections of nucleus angularis and nucleus laminaris to the lateral lemniscal nuclear complex of the barn owl , 1988, The Journal of comparative neurology.

[25]  L F Dell'Osso,et al.  Audio-ocular response characteristics. , 1978, Sensory processes.

[26]  Yunyan Wang,et al.  Population-Wide Bias of Surround Suppression in Auditory Spatial Receptive Fields of the Owl's Midbrain , 2012, The Journal of Neuroscience.

[27]  Y. Gutfreund,et al.  Stimulus-Specific Adaptation: Can It Be a Neural Correlate of Behavioral Habituation? , 2011, The Journal of Neuroscience.

[28]  J A Mazer,et al.  How the owl resolves auditory coding ambiguity. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Harald Luksch,et al.  A Candidate Pathway for a Visual Instructional Signal to the Barn Owl's Auditory System , 2000, The Journal of Neuroscience.

[30]  A J King,et al.  Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: a map of auditory space. , 1987, Journal of neurophysiology.

[31]  T. Yin,et al.  Behavioral Studies of Sound Localization in the Cat , 1998, The Journal of Neuroscience.

[32]  Daniel Guitton,et al.  Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts , 2003, Nature Neuroscience.

[33]  E. Knudsen,et al.  Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn owl , 1990, Nature.

[34]  K. Saberi,et al.  Neural bases of an auditory illusion and its elimination in owls , 1999, Nature Neuroscience.

[35]  B. Gaese,et al.  Coding for auditory space in the superior colliculus of the rat , 2000, The European journal of neuroscience.

[36]  A. John Van Opstal,et al.  Plasticity in human sound localization induced by compressed spatial vision , 2003, Nature Neuroscience.

[37]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  D. Munoz,et al.  On the importance of the transient visual response in the superior colliculus , 2008, Current Opinion in Neurobiology.

[39]  Brian J. Fischer,et al.  Owl's behavior and neural representation predicted by Bayesian inference , 2011, Nature Neuroscience.

[40]  J. Schnupp,et al.  Sound localization behavior in ferrets: Comparison of acoustic orientation and approach-to-target responses , 2008, Neuroscience.

[41]  Eric I Knudsen,et al.  Visual modulation of auditory responses in the owl inferior colliculus. , 2009, Journal of neurophysiology.

[42]  M. Wallace,et al.  Representation and integration of multiple sensory inputs in primate superior colliculus. , 1996, Journal of neurophysiology.

[43]  E I Knudsen,et al.  Characterization of a forebrain gaze field in the archistriatum of the barn owl: microstimulation and anatomical connections , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  James M. Olson,et al.  Gated Visual Input to the Central Auditory System , 2002 .

[45]  Terry T. Takahashi,et al.  Localization and identification of concurrent sounds in the owl’s auditory space map. , 2009 .

[46]  Brian S. Nelson,et al.  Spatial Hearing in Echoic Environments: The Role of the Envelope in Owls , 2010, Neuron.

[47]  E. Knudsen Auditory and visual maps of space in the optic tectum of the owl , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  M. Konishi,et al.  Neural map of interaural phase difference in the owl's brainstem. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Shay Ohayon,et al.  Multiple manifestations of microstimulation in the optic tectum: eye movements, pupil dilations, and sensory priming. , 2010, Journal of neurophysiology.

[50]  Michele A. Basso,et al.  Modulation of neuronal activity by target uncertainty , 1997, Nature.

[51]  H. Wagner,et al.  Improvements of Sound Localization Abilities by the Facial Ruff of the Barn Owl (Tyto alba) as Demonstrated by Virtual Ruff Removal , 2009, PloS one.

[52]  Robert M. McPeek,et al.  Deficits in saccade target selection after inactivation of superior colliculus , 2004, Nature Neuroscience.

[53]  Christopher D. Carello,et al.  Target selection and the superior colliculus: goals, choices and hypotheses , 2004, Vision Research.

[54]  Andrew Moiseff,et al.  Bi-coordinate sound localization by the barn owl , 2004, Journal of Comparative Physiology A.

[55]  Masakazu Konishi,et al.  From Postsynaptic Potentials to Spikes in the Genesis of Auditory Spatial Receptive Fields , 2002, The Journal of Neuroscience.

[56]  Eric I. Knudsen,et al.  Distinct Mechanisms for Top-Down Control of Neural Gain and Sensitivity in the Owl Optic Tectum , 2008, Neuron.

[57]  Masakazu Konishi,et al.  Effects of Interaural Decorrelation on Neural and Behavioral Detection of Spatial Cues , 1998, Neuron.

[58]  C. Blakemore,et al.  Developmental plasticity in the visual and auditory representations in the mammalian superior colliculus , 1988, Nature.

[59]  J I Gold,et al.  Hearing impairment induces frequency-specific adjustments in auditory spatial tuning in the optic tectum of young owls. , 1999, Journal of neurophysiology.

[60]  E. Knudsen,et al.  Signaling of the Strongest Stimulus in the Owl Optic Tectum , 2011, Journal of Neuroscience.

[61]  A Moiseff,et al.  Time and intensity cues are processed independently in the auditory system of the owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  E I Knudsen,et al.  Visual instruction of the neural map of auditory space in the developing optic tectum. , 1991, Science.

[63]  Klaus Hartung,et al.  Head-related transfer functions of the barn owl: measurement and neural responses , 1998, Hearing Research.

[64]  H. Wagner,et al.  Sound-localization deficits induced by lesions in the barn owl's auditory space map [published erratum appears in J Neurosci 1993 Apr;13(4):following table of contents] , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  D. M. Green,et al.  Sound localization by human listeners. , 1991, Annual review of psychology.

[66]  James R Müller,et al.  Microstimulation of the superior colliculus focuses attention without moving the eyes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Eric I. Knudsen,et al.  Multiple Sites of Adaptive Plasticity in the Owl's Auditory Localization Pathway , 2004, The Journal of Neuroscience.

[68]  H Wagner,et al.  Influence of temporal cues on acoustic motion-direction sensitivity of auditory neurons in the owl. , 1992, Journal of neurophysiology.

[69]  Eric I. Knudsen,et al.  Global Inhibition and Stimulus Competition in the Owl Optic Tectum , 2010, The Journal of Neuroscience.