Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat

Essential to spatial orientation in the natural environment is a dynamic representation of direction and distance to objects. Despite the importance of 3D spatial localization to parse objects in the environment and to guide movement, most neurophysiological investigations of sensory mapping have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here, we show for the first time that sensory neurons in the midbrain superior colliculus (SC) of the free-flying echolocating bat encode 3D egocentric space, and that the bat’s inspection of objects in the physical environment sharpens tuning of single neurons, and shifts peak responses to represent closer distances. These findings emerged from wireless neural recordings in free-flying bats, in combination with an echo model that computes the animal’s instantaneous stimulus space. Our research reveals dynamic 3D space coding in a freely moving mammal engaged in a real-world navigation task.

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

[2]  P. Jen,et al.  Auditory response properties and spatial response areas of superior collicular neurons of the FM bat,Eptesicus fuscus , 1984, Journal of Comparative Physiology A.

[3]  H. Schnitzler,et al.  Range estimation by echolocation in the bat Eptesicus fuscus: trading of phase versus time cues. , 1989, The Journal of the Acoustical Society of America.

[4]  N. Suga,et al.  Neural axis representing target range in the auditory cortex of the mustache bat. , 1979, Science.

[5]  Jeffrey C. Erlich,et al.  Requirement of Prefrontal and Midbrain Regions for Rapid Executive Control of Behavior in the Rat , 2015, Neuron.

[6]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[7]  Marion R Van Horn,et al.  Vergence Neurons Identified in the Rostral Superior Colliculus Code Smooth Eye Movements in 3D Space , 2013, The Journal of Neuroscience.

[8]  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.

[9]  N Suga,et al.  Target range-sensitive neurons in the auditory cortex of the mustache bat. , 1979, Science.

[10]  C Blakemore,et al.  Binocular interaction in the cat's superior colliculus. , 1975, The Journal of physiology.

[11]  E. Knudsen,et al.  Control from below: the role of a midbrain network in spatial attention , 2011, The European journal of neuroscience.

[12]  J. Simmons The resolution of target range by echolocating bats. , 1973, The Journal of the Acoustical Society of America.

[13]  Cynthia F. Moss,et al.  Behavioral Studies of Auditory Information Processing , 1995 .

[14]  M. Jerome Beetz,et al.  Cortical neurons of bats respond best to echoes from nearest targets when listening to natural biosonar multi-echo streams , 2016, Scientific Reports.

[15]  D. Ballard,et al.  Eye movements in natural behavior , 2005, Trends in Cognitive Sciences.

[16]  P. T. Madsena,et al.  Recording and quantification of ultrasonic echolocation clicks from free-ranging toothed whales , 2006 .

[17]  J. A. Gisbergen,et al.  Shared target selection for combined version-vergence eye movements. , 1998, Journal of neurophysiology.

[18]  K Hepp,et al.  Monkey superior colliculus represents rapid eye movements in a two-dimensional motor map. , 1993, Journal of neurophysiology.

[19]  Jeremy J. Jay,et al.  Cross-Species Integrative Functional Genomics in GeneWeaver Reveals a Role for Pafah1b1 in Altered Response to Alcohol , 2016, Front. Behav. Neurosci..

[20]  Gidon Felsen,et al.  Neural Substrates of Sensory-Guided Locomotor Decisions in the Rat Superior Colliculus , 2008, Neuron.

[21]  J. Simmons,et al.  Interpulse interval modulation by echolocating big brown bats (Eptesicus fuscus) in different densities of obstacle clutter , 2009, Journal of Comparative Physiology A.

[22]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[23]  J. V. Van Gisbergen,et al.  Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus. , 1999, Journal of neurophysiology.

[24]  J. V. Van Gisbergen,et al.  Stimulation in the rostral pole of monkey superior colliculus: effects on vergence eye movements , 2000, Experimental Brain Research.

[25]  Matthias M. Müller,et al.  Selective visual-spatial attention alters induced gamma band responses in the human EEG , 1999, Clinical Neurophysiology.

[26]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[27]  D L Sparks,et al.  Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. , 1986, Physiological reviews.

[28]  D. Sparks,et al.  Dissociation of visual and saccade-related responses in superior colliculus neurons. , 1980, Journal of neurophysiology.

[29]  C F Moss,et al.  Spatially Selective Auditory Responses in the Superior Colliculus of the Echolocating Bat , 1997, The Journal of Neuroscience.

[30]  Erika E. Fanselow,et al.  Behavioral Modulation of Tactile Responses in the Rat Somatosensory System , 1999, The Journal of Neuroscience.

[31]  Robert Desimone,et al.  Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4 , 2005, Science.

[32]  D. Pélisson,et al.  Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. , 1991, Journal of neurophysiology.

[33]  Richard J Krauzlis,et al.  Changes in perceptual sensitivity related to spatial cues depends on subcortical activity , 2017, Proceedings of the National Academy of Sciences.

[34]  A. Zador,et al.  Auditory cortex mediates the perceptual effects of acoustic temporal expectation , 2010, Nature Neuroscience.

[35]  Ronald L. Calabrese,et al.  A Role for Compromise: Synaptic Inhibition and Electrical Coupling Interact to Control Phasing in the Leech Heartbeat CPG , 2010, Front. Behav. Neurosci..

[36]  Stephen J. Gotts,et al.  High-frequency, Long-range Coupling between Prefrontal and Visual Cortex during Sustained Attention , 2022 .

[37]  Nachum Ulanovsky,et al.  Representation of Three-Dimensional Space in the Hippocampus of Flying Bats , 2013, Science.

[38]  Cynthia F Moss,et al.  Three-dimensional auditory localization in the echolocating bat , 2016, Current Opinion in Neurobiology.

[39]  Alexandre Zénon,et al.  Attention deficits without cortical neuronal deficits , 2012, Nature.

[40]  Eric I. Knudsen,et al.  Top-down gain control of the auditory space map by gaze control circuitry in the barn owl , 2006, Nature.

[41]  Kwabena Boahen,et al.  Space coding by gamma oscillations in the barn owl optic tectum. , 2011, Journal of neurophysiology.

[42]  Cynthia F. Moss,et al.  Probing the Natural Scene by Echolocation in Bats , 2010, Front. Behav. Neurosci..

[43]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[44]  Cynthia F. Moss,et al.  Timing matters: sonar call groups facilitate target localization in bats , 2014, Front. Physiol..

[45]  Margrit Betke,et al.  A protocol and calibration method for accurate multi-camera field videography , 2014, Journal of Experimental Biology.

[46]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

[47]  Daniel Senkowski,et al.  Multisensory processing and oscillatory gamma responses: effects of spatial selective attention , 2005, Experimental Brain Research.

[48]  Min Wu,et al.  Auditory response properties and spatial response areas of single neurons in the pontine nuclei of the big brown bat, Eptesicus fuscus , 1992, Brain Research.

[49]  S. David,et al.  Auditory attention : focusing the searchlight on sound , 2007 .

[50]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[51]  Eric I. Knudsen,et al.  Gamma Oscillations Are Generated Locally in an Attention-Related Midbrain Network , 2012, Neuron.

[52]  R. Krauzlis Recasting the smooth pursuit eye movement system. , 2004, Journal of neurophysiology.

[53]  Shreesh P Mysore,et al.  The role of a midbrain network in competitive stimulus selection , 2011, Current Opinion in Neurobiology.

[54]  Stephen V David,et al.  Rapid Task-Related Plasticity of Spectrotemporal Receptive Fields in the Auditory Midbrain , 2015, The Journal of Neuroscience.

[55]  J. Kobler,et al.  Central acoustic tract in an echolocating bat: An extralemniscal auditory pathway to the thalamus , 1989, The Journal of comparative neurology.

[56]  Luba Sominsky,et al.  Eating behavior and stress: a pathway to obesity , 2014, Front. Psychol..

[57]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[58]  P. Grobstein Between the retinotectal projection and directed movement: topography of a sensorimotor interface. , 1988, Brain, behavior and evolution.

[59]  M. Jerome Beetz,et al.  Temporal tuning in the bat auditory cortex is sharper when studied with natural echolocation sequences , 2016, Scientific Reports.

[60]  Devarajan Sridharan,et al.  Gamma oscillations in the midbrain spatial attention network: linking circuits to function , 2015, Current Opinion in Neurobiology.

[61]  Joseph Krummenacher,et al.  Visual search and attention , 2006 .

[62]  E. Newman,et al.  Integration of visual and infrared information in bimodal neurons in the rattlesnake optic tectum. , 1981, Science.

[63]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[64]  H. Schnitzler,et al.  Accuracy of target ranging in echolocating bats: acoustic information processing , 1989, Journal of Comparative Physiology A.

[65]  Cynthia F. Moss,et al.  Perceiving the World Through Echolocation and Vision , 2016 .

[66]  N Suga,et al.  Delay-tuned combination-sensitive neurons in the auditory cortex of the vocalizing mustached bat. , 1988, Journal of neurophysiology.

[67]  Mark M G Walton,et al.  Discharge of saccade-related superior colliculus neurons during saccades accompanied by vergence. , 2003, Journal of neurophysiology.

[68]  M. Castro-Alamancos,et al.  Neuromodulation of Whisking Related Neural Activity in Superior Colliculus , 2014, The Journal of Neuroscience.

[69]  M S Loop,et al.  Merging of modalities in the optic tectum: infrared and visual integration in rattlesnakes. , 1978, Science.

[70]  D. Ballard,et al.  Eye guidance in natural vision: reinterpreting salience. , 2011, Journal of vision.

[71]  J. C. Middlebrooks,et al.  A neural code for auditory space in the cat's superior colliculus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[72]  A. Feng,et al.  Echo detection and target-ranging neurons in the auditory system of the bat Eptesicus fuscus. , 1978, Science.

[73]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[74]  Herbert Peremans,et al.  Echo-acoustic flow dynamically modifies the cortical map of target range in bats , 2014, Nature Communications.

[75]  I. Matsuo,et al.  Echolocating Big Brown Bats, Eptesicus fuscus, Modulate Pulse Intervals to Overcome Range Ambiguity in Cluttered Surroundings , 2016, Front. Behav. Neurosci..

[76]  Bijan Pesaran,et al.  Neural Correlates of Visual–Spatial Attention in Electrocorticographic Signals in Humans , 2011, Front. Hum. Neurosci..

[77]  C. Moss,et al.  Steering by Hearing: A Bat’s Acoustic Gaze Is Linked to Its Flight Motor Output by a Delayed, Adaptive Linear Law , 2006, The Journal of Neuroscience.

[78]  S. Altmann Rotations, Quaternions, and Double Groups , 1986 .

[79]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[80]  J A Simmons,et al.  Perception of echo phase information in bat sonar. , 1979, Science.

[81]  Jadin C. Jackson,et al.  Quantitative measures of cluster quality for use in extracellular recordings , 2005, Neuroscience.

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

[83]  Lawrence G. McDade,et al.  Behavioral Indices of Multisensory Integration: Orientation to Visual Cues is Affected by Auditory Stimuli , 1989, Journal of Cognitive Neuroscience.

[84]  M. Carrasco Visual attention: The past 25 years , 2011, Vision Research.

[85]  Hans-Ulrich Schnitzler,et al.  Echolocation behaviour of the big brown bat (Eptesicus fuscus) in an obstacle avoidance task of increasing difficulty , 2014, Journal of Experimental Biology.

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

[87]  G. M. Hope,et al.  Electrical response of bat retina to spectral stimulation: comparison of four microchiropteran species , 1979, Experientia.

[88]  Nachum Ulanovsky,et al.  Vectorial representation of spatial goals in the hippocampus of bats , 2017, Science.

[89]  P. Verghese Visual Search and Attention A Signal Detection Theory Approach , 2001, Neuron.

[90]  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.

[91]  Margaret L. Brandeau,et al.  Optimal Localization by Pointing Off Axis , 2010 .

[92]  N. Suga,et al.  Encoding of target range and its representation in the auditory cortex of the mustached bat , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  R. Wurtz,et al.  Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. , 1976, Journal of neurophysiology.

[94]  N. Shimizu [Neurology of eye movements]. , 2000, Rinsho shinkeigaku = Clinical neurology.

[95]  C. Rocha-Miranda,et al.  Disparity selective units in the superior colliculus of the opossum , 2004, Experimental Brain Research.

[96]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[97]  S. Stevenson,et al.  Discrimination of jittered sonar echoes by the echolocating bat, Eptesicus fuscus: The shape of target images in echolocation , 1990, Journal of Comparative Physiology A.

[98]  J. Simmons,et al.  Echolocation and pursuit of prey by bats. , 1979, Science.

[99]  C. Moss,et al.  Active Listening for Spatial Orientation in a Complex Auditory Scene , 2006, PLoS biology.

[100]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[101]  Bruno A. Olshausen,et al.  Scene analysis in the natural environment , 2014, Front. Psychol..

[102]  James A Simmons,et al.  Spatial memory and stereotypy of flight paths by big brown bats in cluttered surroundings , 2013, Journal of Experimental Biology.

[103]  D. Hartley,et al.  The sound emission pattern of the echolocating bat, Eptesicus fuscus , 1989 .

[104]  T. Womelsdorf,et al.  Dynamic shifts of visual receptive fields in cortical area MT by spatial attention , 2006, Nature Neuroscience.

[105]  Cynthia F. Moss,et al.  Bats coordinate sonar and flight behavior as they forage in open and cluttered environments , 2014, Journal of Experimental Biology.

[106]  R. Krauzlis,et al.  Superior colliculus and visual spatial attention. , 2013, Annual review of neuroscience.

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

[108]  C. Moss,et al.  The sonar beam pattern of a flying bat as it tracks tethered insects. , 2003, The Journal of the Acoustical Society of America.

[109]  C F Moss,et al.  Auditory scene analysis by echolocation in bats. , 2001, The Journal of the Acoustical Society of America.

[110]  M. Carandini,et al.  Integration of visual motion and locomotion in mouse visual cortex , 2013, Nature Neuroscience.

[111]  N Suga,et al.  Delay-tuned neurons in the midbrain of the big brown bat. , 1995, Journal of neurophysiology.

[112]  D. Griffin Listening in the dark: The acoustic orientation of bats and men. , 1958 .

[113]  D. Wong Spatial tuning of auditory neurons in the superior colliculus of the echolocating bat, Myotis lucifugus , 1984, Hearing Research.

[114]  Nachum Ulanovsky,et al.  Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation , 2015, Nature Reviews Neuroscience.

[115]  J. Fritz,et al.  Tonotopic and functional organization in the auditory cortex of the big brown bat, Eptesicus fuscus. , 1993, Journal of neurophysiology.

[116]  P. Schiller,et al.  Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. , 1971, Journal of neurophysiology.

[117]  Shiva R. Sinha,et al.  Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus , 2002, Journal of Comparative Physiology A.