Auditory Cortex Spatial Sensitivity Sharpens During Task Performance

Activity in the primary auditory cortex (A1) is essential for normal sound localization behavior, but previous studies of the spatial sensitivity of neurons in A1 have found broad spatial tuning. We tested the hypothesis that spatial tuning sharpens when an animal engages in an auditory task. Cats performed a task that required evaluation of the locations of sounds and one that required active listening, but in which sound location was irrelevant. Some 26–44% of the units recorded in A1 showed substantially sharpened spatial tuning during the behavioral tasks as compared with idle conditions, with the greatest sharpening occurring during the location-relevant task. Spatial sharpening occurred on a scale of tens of seconds and could be replicated multiple times in ∼1.5-h test sessions. Sharpening resulted primarily from increased suppression of responses to sounds at least-preferred locations. That and an observed increase in latencies suggest an important role of inhibitory mechanisms.

[1]  Charles C Lee,et al.  Connections of cat auditory cortex: III. Corticocortical system , 2008, The Journal of comparative neurology.

[2]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[3]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[4]  Virginia Best,et al.  Sound localization with a preceding distractor. , 2007, The Journal of the Acoustical Society of America.

[5]  M. Banks,et al.  Properties of a population of GABAergic cells in murine auditory cortex weakly excited by thalamic stimulation. , 2006, Journal of neurophysiology.

[6]  John C. Middlebrooks,et al.  Directional sensitivity of neurons in the primary auditory (AI) cortex: effects of sound-source intensity level. , 2003, Journal of neurophysiology.

[7]  Jon Driver,et al.  Covert Spatial Orienting in Audition: Exogenous and Endogenous Mechanisms , 1994 .

[8]  D. Alais,et al.  Speech intelligibility reduces over distance from an attended location: Evidence for an auditory spatial gradient of attention , 2009, Attention, perception & psychophysics.

[9]  Mounya Elhilali,et al.  Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields , 2009, Neuron.

[10]  Virginia Best,et al.  Object continuity enhances selective auditory attention , 2008, Proceedings of the National Academy of Sciences.

[11]  John C Middlebrooks,et al.  Spatial sensitivity in the dorsal zone (area DZ) of cat auditory cortex. , 2005, Journal of neurophysiology.

[12]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[13]  D. Kipke,et al.  In vivo stability and biocompatibility of implanted calcium alginate disks. , 2007, Journal of biomedical materials research. Part A.

[14]  André Brechmann,et al.  Hemispheric shifts of sound representation in auditory cortex with conceptual listening. , 2005, Cerebral cortex.

[15]  D. Diamond,et al.  Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. , 1989, Behavioral neuroscience.

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

[17]  Geoffrey M Ghose,et al.  Learning in mammalian sensory cortex , 2004, Current Opinion in Neurobiology.

[18]  J. Edeline,et al.  Tonotopic control of auditory thalamus frequency tuning by reticular thalamic neurons. , 2008, Journal of neurophysiology.

[19]  D. Rasmusson,et al.  Inactivation of prefrontal cortex abolishes cortical acetylcholine release evoked by sensory or sensory pathway stimulation in the rat , 2007, Neuroscience.

[20]  D. M. Green,et al.  A panoramic code for sound location by cortical neurons. , 1994, Science.

[21]  H. Barbas,et al.  Prefrontal Projections to the Thalamic Reticular Nucleus form a Unique Circuit for Attentional Mechanisms , 2006, The Journal of Neuroscience.

[22]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  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.

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

[25]  Xiaoqin Wang,et al.  Sustained firing in auditory cortex evoked by preferred stimuli , 2005, Nature.

[26]  A. Kimura,et al.  Axonal projections of single auditory neurons in the thalamic reticular nucleus: implications for tonotopy‐related gating function and cross‐modal modulation , 2007, The European journal of neuroscience.

[27]  Jun Yan,et al.  Corticothalamic feedback for sound-specific plasticity of auditory thalamic neurons elicited by tones paired with basal forebrain stimulation. , 2008, Cerebral cortex.

[28]  John C Middlebrooks,et al.  Sound localization deficits during reversible deactivation of primary auditory cortex and/or the dorsal zone. , 2008, Journal of neurophysiology.

[29]  Frederick J. Gallun,et al.  The advantage of knowing where to listen. , 2005, The Journal of the Acoustical Society of America.

[30]  B. Moore,et al.  Suggested formulae for calculating auditory-filter bandwidths and excitation patterns. , 1983, The Journal of the Acoustical Society of America.

[31]  M. Merzenich,et al.  Cortical remodelling induced by activity of ventral tegmental dopamine neurons , 2001, Nature.

[32]  Katherine L. Roberts,et al.  Covert auditory spatial orienting: an evaluation of the spatial relevance hypothesis. , 2009, Journal of experimental psychology. Human perception and performance.

[33]  D. M. Green,et al.  Characterization of external ear impulse responses using Golay codes. , 1992, The Journal of the Acoustical Society of America.

[34]  J. C. Middlebrooks,et al.  Cortical representation of auditory space: information-bearing features of spike patterns. , 2002, Journal of neurophysiology.

[35]  R. Zatorre,et al.  Shifting and focusing auditory spatial attention. , 1995, Journal of experimental psychology. Human perception and performance.

[36]  T. Imig,et al.  Single-unit selectivity to azimuthal direction and sound pressure level of noise bursts in cat high-frequency primary auditory cortex. , 1990, Journal of neurophysiology.

[37]  D. Kipke,et al.  Enhanced contrast sensitivity in auditory cortex as cats learn to discriminate sound frequencies. , 2005, Brain research. Cognitive brain research.

[38]  G. Rhodes.  Auditory attention and the representation of spatial information , 1987, Perception & psychophysics.

[39]  Selene Cansino,et al.  Neuromagnetic fields reveal cortical plasticity when learning an auditory discrimination task , 1997, Brain Research.

[40]  Gonzalo H. Otazu,et al.  Engaging in an auditory task suppresses responses in auditory cortex , 2009, Nature Neuroscience.

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

[42]  A. Nuñez,et al.  Electrophysiological evidence for the existence of a posterior cortical–prefrontal–basal forebrain circuitry in modulating sensory responses in visual and somatosensory rat cortical areas , 2003, Neuroscience.

[43]  Michael M Merzenich,et al.  Perceptual Learning Directs Auditory Cortical Map Reorganization through Top-Down Influences , 2006, The Journal of Neuroscience.

[44]  M. Semple,et al.  Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Awake Mongolian Gerbil , 2007, The Journal of Neuroscience.

[45]  Brian H Scott,et al.  Effect of Behavioral Context on Representation of a Spatial Cue in Core Auditory Cortex of Awake Macaques , 2007, The Journal of Neuroscience.

[46]  Robert H Wurtz,et al.  Attentional Modulation of Thalamic Reticular Neurons , 2006, The Journal of Neuroscience.

[47]  L. M. Ward,et al.  Spatial relevance determines facilitatory and inhibitory effects of auditory covert spatial orienting , 1999 .

[48]  Henning Scheich,et al.  Learning-induced plasticity in animal and human auditory cortex , 2005, Current Opinion in Neurobiology.

[49]  Nobuo Suga,et al.  Specific and Nonspecific Plasticity of the Primary Auditory Cortex Elicited by Thalamic Auditory Neurons , 2009, The Journal of Neuroscience.

[50]  D. A. Benson,et al.  Single-unit activity in the auditory cortex of monkeys actively localizing sound sources: Spatial tuning and behavioral dependency , 1981, Brain Research.