Spatial interaction between spectral integration and frequency gradient in primary auditory cortex.

Primary sensory cortical areas are characterized by orderly and largely independent representations of several receptive field properties. This is expressed in multiple, spatially overlaying parameter distributions, such as orientation preference, spatial frequency, and ocular dominance maps in the primary visual cortex. In the auditory cortex, two main and presumably independent representational parameters are the center frequency and the frequency extent of spectral tuning curves. Here we demonstrate interactions between cortical tonotopic gradient and spectral bandwidth modules in cat primary auditory cortex (AI). First, the spatial representation of spectral integration is not equally expressed across the whole frequency range in AI. Narrow-bandwidth modules are found only in the mid-frequency region (5-20 kHz). Thus spectral integration properties delineate three frequency regions (<5, 5-20, and >20 kHz) in cat AI. Second, the extent of spectral integration covaries with the local tonotopic gradient in the low- and mid-frequency ranges. Regions with a shallow frequency gradient tend to have narrower spectral integration than those with a steep gradient. These relationships between spectral selectivity and frequency gradient constrain forebrain models of thalamo- and corticocortical convergence and connectivity and may reflect the processing of behaviorally relevant stimulus constellations.

[1]  C E Schreiner,et al.  Functional topography of cat primary auditory cortex: distribution of integrated excitation. , 1990, Journal of neurophysiology.

[2]  Lee M. Miller,et al.  Functional Convergence of Response Properties in the Auditory Thalamocortical System , 2001, Neuron.

[3]  J. Pickles,et al.  Normal critical bands in the cat. , 1975, Acta oto-laryngologica.

[4]  J. Eggermont,et al.  Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex , 2006, Nature Neuroscience.

[5]  J. Kelly,et al.  Organization of auditory cortex in the albino rat: binaural response properties. , 1988, Journal of neurophysiology.

[6]  P. Knight,et al.  Representation of the cochlea within the anterior auditory field (AAF) of the cat , 1977, Brain Research.

[7]  T. Yin,et al.  Acoustic behavior and midbrain function , 2005 .

[8]  M. Ruggero,et al.  Frequency tuning of basilar membrane and auditory nerve fibers in the same cochleae. , 1998, Science.

[9]  Nobuo Suga,et al.  Sharpening of frequency tuning by inhibition in the central auditory system: tribute to Yasuji Katsuki , 1995, Neuroscience Research.

[10]  Israel Nelken,et al.  Feature Detection by the Auditory Cortex , 2002 .

[11]  J. Eggermont Between sound and perception: reviewing the search for a neural code , 2001, Hearing Research.

[12]  C. Schreiner,et al.  Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. , 1991, Journal of neurophysiology.

[13]  Nicholas J. Priebe,et al.  Modular functional organization of cat anterior auditory field. , 2004, Journal of neurophysiology.

[14]  M. Bushnell,et al.  Pain perception: is there a role for primary somatosensory cortex? , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Palmer,et al.  Interconnections of auditory areas in the guinea pig neocortex , 2002, Experimental Brain Research.

[16]  C E Schreiner,et al.  Topography of excitatory bandwidth in cat primary auditory cortex: single-neuron versus multiple-neuron recordings. , 1992, Journal of neurophysiology.

[17]  J. Arezzo,et al.  Binaural interactions in primary auditory cortex of the awake macaque. , 2000, Cerebral cortex.

[18]  M. Liberman,et al.  Auditory-nerve response from cats raised in a low-noise chamber. , 1978, The Journal of the Acoustical Society of America.

[19]  Shigeto Furukawa,et al.  Location Signaling by Cortical Neurons , 2002 .

[20]  Hideki Kawai,et al.  Spectral integration in auditory cortex: Mechanisms and modulation , 2005, Hearing Research.

[21]  C E Schreiner,et al.  Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Richard R. Fay,et al.  Integrative Functions in the Mammalian Auditory Pathway , 2002, Springer Handbook of Auditory Research.

[23]  D. D. Greenwood A cochlear frequency-position function for several species--29 years later. , 1990, The Journal of the Acoustical Society of America.

[24]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[25]  D. Fitzpatrick,et al.  Spatial coding of position and orientation in primary visual cortex , 2002, Nature Neuroscience.

[26]  G. Recanzone,et al.  Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey , 1999, The Journal of comparative neurology.

[27]  C. Schreiner,et al.  Organization of inhibitory frequency receptive fields in cat primary auditory cortex. , 1999, Journal of neurophysiology.

[28]  C. Schreiner,et al.  Modular organization of frequency integration in primary auditory cortex. , 2000, Annual review of neuroscience.

[29]  C E Schreiner,et al.  Basic functional organization of second auditory cortical field (AII) of the cat. , 1984, Journal of neurophysiology.

[30]  C E Schreiner,et al.  Functional organization of squirrel monkey primary auditory cortex: responses to pure tones. , 2001, Journal of neurophysiology.

[31]  G M Clark,et al.  Critical bands following the selective destruction of cochlear inner and outer hair cells. , 1979, Acta oto-laryngologica.

[32]  T. Imig,et al.  Binaural columns in the primary field (A1) of cat auditory cortex , 1977, Brain Research.

[33]  T. Hashikawa,et al.  Connections of the dorsal zone of cat auditory cortex , 1998, The Journal of comparative neurology.

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

[35]  M. Stryker,et al.  Spatial Frequency Maps in Cat Visual Cortex , 2000, The Journal of Neuroscience.

[36]  A. King,et al.  Auditory function: Neurobiological bases of hearing G.M. Edelman W.E. , 1990, Neuroscience.

[37]  Amiram Grinvald,et al.  Visual cortex maps are optimized for uniform coverage , 2000, Nature Neuroscience.

[38]  J. Winer,et al.  Auditory thalamocortical projections in the cat: Laminar and areal patterns of input , 2000, The Journal of comparative neurology.

[39]  D. P. Phillips,et al.  Level-dependent representation of stimulus frequency in cat primary auditory cortex , 2004, Experimental Brain Research.

[40]  C. Schreiner,et al.  Frequency resolution and spectral integration (critical band analysis) in single units of the cat primary auditory cortex , 1997, Journal of Comparative Physiology A.

[41]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

[42]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[43]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[44]  K. A. Davis,et al.  Circuitry and Function of the Dorsal Cochlear Nucleus , 2002 .

[45]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

[46]  A. Grinvald,et al.  Spatial Relationships among Three Columnar Systems in Cat Area 17 , 1997, The Journal of Neuroscience.

[47]  John Edward Lennard-Jones,et al.  The determination of molecular orbitals , 1949, Proceedings of the Royal Society of London. Series A. Mathematical and Physical Sciences.

[48]  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.

[49]  Li I. Zhang,et al.  Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. , 2004, Journal of neurophysiology.

[50]  Ralph E Beitel,et al.  Functional organization and hemispheric comparison of primary auditory cortex in the common marmoset (Callithrix jacchus) , 2005, The Journal of comparative neurology.

[51]  T. Imig,et al.  Sources and terminations of callosal axons related to binaural and frequency maps in primary auditory cortex of the cat , 1978, The Journal of comparative neurology.

[52]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[53]  J. Winer,et al.  Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI) , 1994, The Journal of comparative neurology.