Mechanisms of Sound Localization in Two Functionally Distinct Regions of the Auditory Cortex

The auditory cortex is necessary for sound localization. The mechanisms that shape bicoordinate spatial representation in the auditory cortex remain unclear. Here, we addressed this issue by quantifying spatial receptive fields (SRFs) in two functionally distinct cortical regions in the pallid bat. The pallid bat uses echolocation for obstacle avoidance and listens to prey-generated noise to localize prey. Its cortex contains two segregated regions of response selectivity that serve echolocation and localization of prey-generated noise. The main aim of this study was to compare 2D SRFs between neurons in the noise-selective region (NSR) and the echolocation region [frequency-modulated sweep-selective region (FMSR)]. The data reveal the following major differences between these two regions: (1) compared with NSR neurons, SRF properties of FMSR neurons were more strongly dependent on sound level; (2) as a population, NSR neurons represent a broad region of contralateral space, while FMSR selectivity was focused near the midline at sound levels near threshold and expanded considerably with increasing sound levels; and (3) the SRF size and centroid elevation were correlated with the characteristic frequency in the NSR, but not the FMSR. These data suggest different mechanisms of sound localization for two different behaviors. Previously, we reported that azimuth is represented by predictable changes in the extent of activated cortex. The present data indicate how elevation constrains this activity pattern. These data suggest a novel model for bicoordinate spatial representation that is based on the extent of activated cortex resulting from the overlap of binaural and tonotopic maps. SIGNIFICANCE STATEMENT Unlike the visual and somatosensory systems, spatial information is not directly represented at the sensory receptor epithelium in the auditory system. Spatial locations are computed by integrating neural binaural properties and frequency-dependent pinna filtering, providing a useful model to study how neural properties and peripheral structures are adapted for sensory encoding. Although auditory cortex is necessary for sound localization, our understanding of how the cortex represents space remains rudimentary. Here we show that two functionally distinct regions of the pallid bat auditory cortex represent 2D space using different mechanisms. In addition, we suggest a novel hypothesis on how the nature of overlap between systematic maps of binaural and frequency selectivity leads to representation of both azimuth and elevation.

[1]  M. Holderied,et al.  Hemprich’s long-eared bat (Otonycteris hemprichii) as a predator of scorpions: whispering echolocation, passive gleaning and prey selection , 2011, Journal of Comparative Physiology A.

[2]  A. King,et al.  Encoding of virtual acoustic space stimuli by neurons in ferret primary auditory cortex. , 2005, Journal of neurophysiology.

[3]  L. Aitkin,et al.  Azimuthal sensitivity of neurons in primary auditory cortex of cats. II. Organization along frequency-band strips. , 1990, Journal of neurophysiology.

[4]  Z M Fuzessery,et al.  Speculations on the role of frequency in sound localization. , 1986, Brain, behavior and evolution.

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

[6]  Z. Fuzessery,et al.  Functional organization of the pallid bat auditory cortex: emphasis on binaural organization. , 2002, Journal of neurophysiology.

[7]  K. Razak,et al.  Parvalbumin and calbindin expression in parallel thalamocortical pathways in a gleaning bat, Antrozous pallidus , 2014, The Journal of comparative neurology.

[8]  Z. Fuzessery,et al.  Monaural and binaural spectral cues created by the external ears of the pallid bat , 1996, Hearing Research.

[9]  Jiping Zhang,et al.  Response patterns along an isofrequency contour in cat primary auditory cortex (AI) to stimuli varying in average and interaural levels. , 2004, Journal of neurophysiology.

[10]  K. Razak Systematic Representation of Sound Locations in the Primary Auditory Cortex , 2011, The Journal of Neuroscience.

[11]  J. R. Barber,et al.  Can two streams of auditory information be processed simultaneously? Evidence from the gleaning bat Antrozous pallidus , 2003, Journal of Comparative Physiology A.

[12]  Z. Fuzessery,et al.  GABA shapes selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex. , 2009, Journal of neurophysiology.

[13]  K. Koka,et al.  Interaural Level Difference Discrimination Thresholds for Single Neurons in the Lateral Superior Olive , 2008, The Journal of Neuroscience.

[14]  Z. Fuzessery,et al.  GABA shapes a systematic map of binaural sensitivity in the auditory cortex. , 2010, Journal of neurophysiology.

[15]  K. Razak Mechanisms underlying azimuth selectivity in the auditory cortex of the pallid bat , 2012, Hearing Research.

[16]  D. Irvine,et al.  Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: implications for auditory spatial representation. , 1985, Journal of neurophysiology.

[17]  B. Grothe,et al.  Precise inhibition is essential for microsecond interaural time difference coding , 2002, Nature.

[18]  J. L. Ruhland,et al.  The role of spectral composition of sounds on the localization of sound sources by cats. , 2013, Journal of neurophysiology.

[19]  D. McAlpine,et al.  A neural code for low-frequency sound localization in mammals , 2001, Nature Neuroscience.

[20]  J. C. Middlebrooks,et al.  Sensitivity to sound-source elevation in nontonotopic auditory cortex. , 1998, Journal of neurophysiology.

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

[22]  J. C. Middlebrooks,et al.  Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  G. Bell Behavioral and ecological aspects of gleaning by a desert insectivorous bat Antrozous pallidus (Chiroptera: Vespertilionidae) , 1982, Behavioral Ecology and Sociobiology.

[24]  Z. M. Fuzessery,et al.  A representation of horizontal sound location in the inferior colliculus of the mustache bat (Pteronotus p. parnellii) , 1985, Hearing Research.

[25]  Stephen G Lomber,et al.  Cortical control of sound localization in the cat: unilateral cooling deactivation of 19 cerebral areas. , 2004, Journal of neurophysiology.

[26]  Z. Fuzessery Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus. , 1994, Journal of neurophysiology.

[27]  Z. Fuzessery,et al.  Facilitatory Mechanisms Underlying Selectivity for the Direction and Rate of Frequency Modulated Sweeps in the Auditory Cortex , 2008, The Journal of Neuroscience.

[28]  A. J. King,et al.  Role of auditory cortex in sound localization in the midsagittal plane. , 2007, Journal of neurophysiology.

[29]  R. Lindsay,et al.  Listening in the Dark , 1958 .

[30]  Lee M. Miller,et al.  Populations of auditory cortical neurons can accurately encode acoustic space across stimulus intensity , 2009, Proceedings of the National Academy of Sciences.

[31]  Robert A. A. Campbell,et al.  Physiological and behavioral studies of spatial coding in the auditory cortex , 2007, Hearing Research.

[32]  M. Merzenich,et al.  Role of cat primary auditory cortex for sound-localization behavior. , 1984, Journal of neurophysiology.

[33]  Rick L Jenison,et al.  Directional Sensitivity of Neurons in the Primary Auditory ( AI ) Cortex : Effects of Sound-Source Intensity Level , 2003 .

[34]  J. Kelly,et al.  Contribution of auditory cortex to sound localization by the ferret (Mustela putorius). , 1987, Journal of neurophysiology.

[35]  Z. Fuzessery,et al.  Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat. , 2006, Journal of neurophysiology.

[36]  H. Heffner,et al.  The role of macaque auditory cortex in sound localization. , 1997, Acta oto-laryngologica. Supplementum.

[37]  T. O'Shea,et al.  Nocturnal and Seasonal Activities of the Pallid Bat, Antrozous Pallidus , 1977 .

[38]  J. C. Middlebrooks,et al.  Location Coding by Opponent Neural Populations in the Auditory Cortex , 2005, PLoS biology.

[39]  J Cranford,et al.  Effects of unilateral ablation of auditory cortex in cat on complex sound localization. , 1972, Journal of neurophysiology.

[40]  Z. Fuzessery,et al.  Parallel thalamocortical pathways for echolocation and passive sound localization in a gleaning bat, Antrozous pallidus , 2007, The Journal of comparative neurology.