Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.

The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA A-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on caudomedial nidopallium (NCM), an area analogous to parts of the mammalian auditory cortex with selective responses to birdsong. We present evidence that GABA A-mediated inhibition plays a pronounced role in NCM's auditory processing of birdsong. Using immunocytochemistry, we show that approximately half of NCM's neurons are GABAergic. Whole cell patch-clamp recordings in a slice preparation demonstrate that, at rest, spontaneously active GABAergic synapses inhibit excitatory inputs onto NCM neurons via GABA A receptors. Multi-electrode electrophysiological recordings in awake birds show that local blockade of GABA A-mediated inhibition in NCM markedly affects the temporal pattern of song-evoked responses in NCM without modifications in frequency tuning. Surprisingly, this blockade increases the phasic and largely suppresses the tonic response component, reflecting dynamic relationships of inhibitory networks that could include disinhibition. Thus processing of learned natural communication sounds in songbirds, and possibly other vocal learners, may depend on complex interactions of inhibitory networks.

[1]  J. Winer,et al.  Evolution of GABAergic circuitry in the mammalian medial geniculate body. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[2]  G. Manley,et al.  Auditory processing in birds , 2000, Current Opinion in Neurobiology.

[3]  Anil Kumar,et al.  Acoustic communication in birds , 2003 .

[4]  H. Karten,et al.  The Origins of Neocortex: Connections and Lamination as Distinct Events in Evolution , 1989, Journal of Cognitive Neuroscience.

[5]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[6]  David S Vicario,et al.  Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[7]  G. Stuart,et al.  Excitatory Actions of GABA in the Cortex , 2003, Neuron.

[8]  E. Jarvis,et al.  Learned Birdsong and the Neurobiology of Human Language , 2004, Annals of the New York Academy of Sciences.

[9]  R. Nicoll,et al.  Pre- and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties , 1988, Neuron.

[10]  E. Jarvis,et al.  Differential expression of glutamate receptors in avian neural pathways for learned vocalization , 2004, The Journal of comparative neurology.

[11]  L. Hughes,et al.  Age-Related Changes in the Inhibitory Response Properties of Dorsal Cochlear Nucleus Output Neurons: Role of Inhibitory Inputs , 2005, The Journal of Neuroscience.

[12]  A. Sillito The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. , 1975, The Journal of physiology.

[13]  Fernando Nottebohm,et al.  Descending auditory pathways in the adult male zebra finch (Taeniopygia Guttata) , 1998, The Journal of comparative neurology.

[14]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[15]  Peter Marler,et al.  Behavioral neurobiology of birdsong , 2004 .

[16]  A. Sillito Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex , 1977, The Journal of physiology.

[17]  P. Jen,et al.  GABAergic disinhibition affects responses of bat inferior collicular neurons to temporally patterned sound pulses. , 1998, Journal of neurophysiology.

[18]  P. Slater,et al.  Bird Song: Biological Themes and Variations , 1995 .

[19]  M. Hauser,et al.  The design of animal communication , 1999 .

[20]  V. Kotak,et al.  A Developmental Shift from GABAergic to Glycinergic Transmission in the Central Auditory System , 1998, The Journal of Neuroscience.

[21]  M. Raiteri,et al.  International Union of Pharmacology. XXXIII. Mammalian γ-Aminobutyric AcidB Receptors: Structure and Function , 2002, Pharmacological Reviews.

[22]  Raphael Pinaud,et al.  GABAergic neurons participate in the brain's response to birdsong auditory stimulation , 2004, The European journal of neuroscience.

[23]  H. Karten,et al.  Connections of the auditory forebrain in the pigeon (columba livia) , 1993, The Journal of comparative neurology.

[24]  P. Jen,et al.  Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons , 1999, Journal of Comparative Physiology A.

[25]  E. Knudsen,et al.  Functional selection of adaptive auditory space map by GABAA-mediated inhibition. , 1999, Science.

[26]  A. Sillito Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. , 1979, The Journal of physiology.

[27]  N Suga,et al.  Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. , 1997, Journal of neurophysiology.

[28]  S J Chew,et al.  A large-capacity memory system that recognizes the calls and songs of individual birds. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[29]  G. Tamás,et al.  Identified Sources and Targets of Slow Inhibition in the Neocortex , 2003, Science.

[30]  K. Albus,et al.  Baclofen inhibits the spontaneous and visually evoked responses of neurones in the striate cortex of the cat , 1987, Neuroscience Letters.

[31]  R. Miles,et al.  On the Origin of Interictal Activity in Human Temporal Lobe Epilepsy in Vitro , 2002, Science.

[32]  Johan J Bolhuis,et al.  An Analysis of the Neural Representation of Birdsong Memory , 2004, The Journal of Neuroscience.

[33]  J. Bolhuis,et al.  Localized neuronal activation in the zebra finch brain is related to the strength of song learning. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  E. Knudsen,et al.  GABAergic Inhibition Antagonizes Adaptive Adjustment of the Owl's Auditory Space Map during the Initial Phase of Plasticity , 2001, The Journal of Neuroscience.

[35]  David S Vicario,et al.  Auditory topography and temporal response dynamics of canary caudal telencephalon. , 2006, Journal of neurobiology.

[36]  M. Raiteri,et al.  International Union of Pharmacology. XXXIII. Mammalian gamma-aminobutyric acid(B) receptors: structure and function. , 2002, Pharmacological reviews.

[37]  D. Vicario,et al.  Song presentation induces gene expression in the songbird forebrain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[38]  G. Pollak,et al.  The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus , 1993, Hearing Research.

[39]  R. Nicoll,et al.  A physiological role for GABAB receptors in the central nervous system , 1988, Nature.

[40]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[41]  R. D. Freeman,et al.  Blockade of intracortical inhibition in kitten striate cortex: Effects on receptive field properties and associated loss of ocular dominance plasticity , 2004, Experimental Brain Research.

[42]  C. Fiorillo,et al.  Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons , 1998, Nature.

[43]  D. Vicario,et al.  Species differences in auditory processing dynamics in songbird auditory telencephalon , 2007, Developmental neurobiology.

[44]  M. Konishi,et al.  Effects of deafening on song development in American robins and black-headed grosbeaks. , 1965, Zeitschrift fur Tierpsychologie.

[45]  R. Dykes,et al.  Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. , 1984, Journal of neurophysiology.

[46]  M. Konishi The role of auditory feedback in the control of vocalization in the white-crowned sparrow. , 1965, Zeitschrift fur Tierpsychologie.

[47]  C. Müller,et al.  Feature extraction and tonotopic organization in the avian auditory forebrain , 2004, Experimental Brain Research.

[48]  C. G. Benson,et al.  Plastic Changes in Glycine and GABA Release and Uptake in Adult Brain Stem Auditory Nuclei after Unilateral Middle Ear Ossicle Removal and Cochlear Ablation , 1998, Experimental Neurology.

[49]  G D Pollak,et al.  GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. , 1992, Journal of neurophysiology.

[50]  S. Nowicki,et al.  Song Function and the Evolution of Female Preferences: Why Birds Sing, Why Brains Matter , 2004, Annals of the New York Academy of Sciences.

[51]  C. Mello,et al.  Calbindin-positive neurons reveal a sexual dimorphism within the songbird analogue of the mammalian auditory cortex. , 2006, Journal of neurobiology.

[52]  G. E. Vates,et al.  Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata) , 1996, The Journal of comparative neurology.

[53]  K. Sen,et al.  Feature analysis of natural sounds in the songbird auditory forebrain. , 2001, Journal of neurophysiology.

[54]  R. Nicoll,et al.  GABA Generates Excitement , 2003, Neuron.

[55]  P. Jen,et al.  Bicuculline application affects discharge patterns, rate–intensity functions, and frequency tuning characteristics of bat auditory cortical neurons , 2000, Hearing Research.

[56]  C. Mello,et al.  GABA immunoreactivity in auditory and song control brain areas of zebra finches , 2007, Journal of Chemical Neuroanatomy.

[57]  Liisa A. Tremere,et al.  Expansion of receptive fields in raccoon somatosensory cortex in vivo by GABAA receptor antagonism: implications for cortical reorganization , 2001, Experimental Brain Research.

[58]  Johan J. Bolhuis,et al.  Birdsong Memory: A Neural Dissociation between Song Recognition and Production , 2007, Current Biology.

[59]  Clifford B Saper,et al.  Magic peptides, magic antibodies: Guidelines for appropriate controls for immunohistochemistry , 2003, The Journal of comparative neurology.

[60]  Darrell R. Abernethy,et al.  International Union of Pharmacology: Approaches to the Nomenclature of Voltage-Gated Ion Channels , 2003, Pharmacological Reviews.

[61]  J. Walrond,et al.  Two structural adaptations for regulating transmitter release at lobster neuromuscular synapses , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  N. A. Lazareva,et al.  Orientation tuning and receptive field structure in cat striate neurons during local blockade of intracortical inhibition , 1998, Neuroscience.