Prediction of auditory spatial acuity from neural images on the owl's auditory space map

The owl can discriminate changes in the location of sound sources as small as 3° and can aim its head to within 2° of a source. A typical neuron in its midbrain space map has a spatial receptive field that spans 40°—a width that is many times the behavioural threshold. Here we have quantitatively examined the relationship between neuronal activity and perceptual acuity in the auditory space map in the barn owl midbrain. By analysing changes in firing rate resulting from small changes of stimulus azimuth, we show that most neurons can reliably signal changes in source location that are smaller than the behavioural threshold. Each source is represented in the space map by a focus of activity in a population of neurons. Displacement of the source causes the pattern of activity in this population to change. We show that this change predicts the owl's ability to detect a change in source location.

[1]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[2]  J. Gold,et al.  Representation of a perceptual decision in developing oculomotor commands , 2000, Nature.

[3]  M. Ahissar,et al.  Encoding of sound-source location and movement: activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex. , 1992, Journal of neurophysiology.

[4]  Curtis C Bell,et al.  Memory-based expectations in electrosensory systems , 2001, Current Opinion in Neurobiology.

[5]  E. N. Sokolov Higher nervous functions; the orienting reflex. , 1963, Annual review of physiology.

[6]  G H Recanzone,et al.  Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the macaque monkey. , 2000, Journal of neurophysiology.

[7]  M F Land,et al.  The knowledge base of the oculomotor system. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[9]  D. Ballard,et al.  Memory Representations in Natural Tasks , 1995, Journal of Cognitive Neuroscience.

[10]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Michael F. Land,et al.  From eye movements to actions: how batsmen hit the ball , 2000, Nature Neuroscience.

[12]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[13]  P. A. Kolers Recognizing patterns , 1968 .

[14]  K. J. Cole,et al.  Sensory-motor coordination during grasping and manipulative actions , 1992, Current Biology.

[15]  K. H. Britten,et al.  Spatial Summation in the Receptive Fields of MT Neurons , 1999, The Journal of Neuroscience.

[16]  R. Hari,et al.  Modulated Activation of the Human SI and SII Cortices during Observation of Hand Actions , 2002, NeuroImage.

[17]  E I Knudsen,et al.  Receptive fields of auditory neurons in the owl. , 1977, Science.

[18]  G. Rizzolatti,et al.  I Know What You Are Doing A Neurophysiological Study , 2001, Neuron.

[19]  R. Hari,et al.  Temporal dynamics of cortical representation for action. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[20]  P. B. Farel,et al.  Habituation of a monosynaptic response in frog spinal cord: evidence for a presynaptic mechanism. , 1976, Journal of neurophysiology.

[21]  I. Fujita,et al.  The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  W. Heiligenberg,et al.  How sensory maps could enhance resolution through ordered arrangements of broadly tuned receivers , 2004, Biological Cybernetics.

[23]  Helmut Schwegler,et al.  Coarse coding: calculation of the resolution achieved by a population of large receptive field neurons , 1997, Biological Cybernetics.

[24]  R. Johansson,et al.  Eye–Hand Coordination in Object Manipulation , 2001, The Journal of Neuroscience.

[25]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[26]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[27]  J L HALL,et al.  Binaural interaction in the accessory superior olivary nucleus of the cat - an electrophysiological study of single neurons , 1963, The Journal of the Acoustical Society of America.

[28]  E R Kandel,et al.  A common presynaptic locus for the synaptic changes underlying short-term habituation and sensitization of the gill-withdrawal reflex in Aplysia. , 1976, Cold Spring Harbor symposia on quantitative biology.

[29]  E. Rolls,et al.  Neural networks and brain function , 1998 .

[30]  Masakazu Konishi,et al.  Mechanisms of sound localization in the barn owl (Tyto alba) , 1979, Journal of comparative physiology.

[31]  R. H. Arnott,et al.  Interaural Time Difference Discrimination Thresholds for Single Neurons in the Inferior Colliculus of Guinea Pigs , 2003, The Journal of Neuroscience.

[32]  G. Rizzolatti,et al.  Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons , 2002, Science.

[33]  J C Mazziotta,et al.  Reafferent copies of imitated actions in the right superior temporal cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Terrence R. Stanford,et al.  A neuronal population code for sound localization , 1997, Nature.

[35]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[37]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[38]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[39]  G. Rizzolatti,et al.  Activation of human primary motor cortex during action observation: a neuromagnetic study. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  A. D. S. Bala,et al.  Pupillary dilation response as an indicator of auditory discrimination in the barn owl , 2000, Journal of Comparative Physiology A.

[41]  E. Rolls,et al.  Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey , 1989, The European journal of neuroscience.

[42]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[43]  B. Sakitt Indices of Discriminability , 1973, Nature.

[44]  J. Mazziotta,et al.  Modulation of motor and premotor activity during imitation of target-directed actions. , 2002, Cerebral cortex.

[45]  H B Barlow,et al.  Single units and sensation: a neuron doctrine for perceptual psychology? , 1972, Perception.

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

[47]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[48]  D H Ballard,et al.  Hand-eye coordination during sequential tasks. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  R. O’Reilly,et al.  Opinion TRENDS in Cognitive Sciences Vol.6 No.12 December 2002 , 2022 .

[50]  Á. Pascual-Leone,et al.  Phase-specific modulation of cortical motor output during movement observation , 2001, Neuroreport.

[51]  T. Paus,et al.  Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study , 2000, Neuroreport.

[52]  H S Colburn,et al.  Theory of binaural interaction based on auditory-nerve data. I. General strategy and preliminary results on interaural discrimination. , 1973, The Journal of the Acoustical Society of America.

[53]  G. Rizzolatti,et al.  Resonance behaviors and mirror neurons. , 1999, Archives italiennes de biologie.

[54]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[55]  M. Land,et al.  The Roles of Vision and Eye Movements in the Control of Activities of Daily Living , 1998, Perception.

[56]  G. Rizzolatti,et al.  Localization of grasp representations in humans by PET: 1. Observation versus execution , 1996, Experimental Brain Research.

[57]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[58]  M. Matarić,et al.  Fixation behavior in observation and imitation of human movement. , 1998, Brain research. Cognitive brain research.

[59]  E. Procyk,et al.  Brain activity during observation of actions. Influence of action content and subject's strategy. , 1997, Brain : a journal of neurology.