The dominant role of inhibition in creating response selectivities for communication calls in the brainstem auditory system

Hearing Research

Volumn 305, Issue 1, 2013, Pages 86-101

  Pollak, George D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN;

AUDITORY NERVOUS SYSTEM; BRAIN STEM; CELL NUCLEUS; CELL POPULATION; CONCEPT FORMATION; DORSAL NUCLEUS OF THE LATERAL LEMNISCUS; EVOKED AUDITORY RESPONSE; INFERIOR COLLICULUS; MESENCEPHALON; NERVE CELL; NERVE TRACT; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; VERBAL COMMUNICATION;

DNLL; DORSAL NUCLEUS OF THE LATERAL LEMNISCUS; EPSP; EXCITATORY POST-SYNAPTIC POTENTIAL; FM; FREQUENCY MODULATION; IC; INFERIOR COLLICULUS; INHIBITORY POST-SYNAPTIC POTENTIAL; IPSP; MEGAOHM; MILLIVOLT; MV; MΩ; POST-SYNAPTIC POTENTIAL; PSP; SI; SIMILARITY INDEX; SPECTROTEMPORAL RECEPTIVE FIELD; STRF;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; BRAIN STEM; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; INFERIOR COLLICULI; NEURAL INHIBITION; PATTERN RECOGNITION, PHYSIOLOGICAL; REACTION TIME; SEROTONIN; SPECIES SPECIFICITY; SYNAPTIC TRANSMISSION; TIME FACTORS; VOCALIZATION, ANIMAL;

EID: 84887020213     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2013.03.001     Document Type: Review

References (63)

1. Andoni S., Pollak G.D. Selectivity for spectral motion as a neural computation for encoding natural communication signals in bat inferior colliculus. J.Neurosci. 2011, 31:16529-16540.
2. Andoni S., Li N., Pollak G.D. Spectrotemporal receptive fields in the inferior colliculus revealing selectivity for spectral motion in conspecific vocalizations. J.Neurosci. 2007, 27:4882-4893.
3. Bauer E.E., Klug A., Pollak G.D. Spectral determination of responses to species-specific calls in the dorsal nucleus of the lateral lemniscus. J.Neurophysiol. 2002, 88:1955-1967.
4. Behr O., von Helversen O. Bat serenades-complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav. Ecol. Sociobiol. 2004, 56:106-115.
5. Bohn K.M., Schmidt-French B., Ma S.T., Pollak G.D. Syllable acoustics, temporal patterns, and call composition vary with behavioral context in Mexican free-tailed bats. J.Acoust. Soc. Am. 2008, 124:1838-1848.
6. Bohn K.M., Schmidt-French B., Schwartz C., Smotherman M., Pollak G.D. Versatility and stereotypy of free-tailed bat songs. PLoS One 2009, 4:e6746.
7. Brimijoin W.O., O'Neill W.E. On the prediction of sweep rate and directional selectivity for FM sounds from two-tone interactions in the inferior colliculus. Hear. Res. 2005, 210:63-79.
8. Casseday J.H., Fremouw T., Covey E. The inferior colliculus: a hub for the central auditory system. Integrative Functions in the Mammalian Auditory Pathway 2002, vol. 15:238-318. Springer-Verlag, New York.
9. Covey E., Casseday J.H. Timing in the auditory system of the bat. Annu. Rev. Physiol. 1999, 61:457-476.
10. Doupe A.J., Kuhl P.K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 1999, 22:567-631.
11. Eeuwes L., Holstrom L., Portfors C. Duration Selectivity Underlies Responses to Social Vocalizations in the IC 2009, 218. Abstracts, Association for Research in Otolarynology Midwinter Meeting 32.
12. Felix R.A., Portfors C.V. Excitatory, inhibitory and facilitatory frequency response areas in the inferior colliculus of hearing impaired mice. Hear. Res. 2007, 228:212-229.
13. Fuzessery Z.M., Hall J.C. Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J.Neurophysiol. 1996, 76:1059-1073.
14. Fuzessery Z.M., Richardson M.D., Coburn M.S. Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the inferior colliculus of the pallid bat. J.Neurophysiol. 2006, 96:1320-1336.
15. Fuzessery Z.M., Razak K.A., Williams A.J. Multiple mechanisms shape selectivity for FM sweep rate and direction in the pallid bat inferior colliculus and auditory cortex. J.Comp. Physiol. A Neuroethol Sens Neural Behav. Physiol. 2011, 197:615-623.
16. Gittelman J.X., Li N. FM velocity selectivity in the inferior colliculus is inherited from velocity-selective inputs and enhanced by spike threshold. J.Neurophysiol. 2010, 106:2399-2414.
17. Gittelman J.X., Pollak G.D. It's about time: how input timing is used and not used to create emergent properties in the auditory system. J.Neurosci. 2011, 31:2576-2583.
18. Gittelman J.X., Wang L., Colburn H.S., Pollak G.D. Inhibition shapes response selectivity in the inferior colliculus by gain modulation. Front. Neural Circuits 2012, 6:67.
19. Gittelman J.X., Li N., Pollak G.D. Mechanisms underlying directional selectivity for frequency modulated sweeps in the inferior colliculus revealed by invivo whole-cell recordings. J.Neurosci. 2009, 29:13030-13041.
20. Holmstrom L., Roberts P.D., Portfors C.V. Responses to social vocalizations in the inferior colliculus of the mustached bat are influenced by secondary tuning curves. J.Neurophysiol. 2007, 98:3461-3472.
21. Hurley L.M. Different serotonin receptor agonists have distinct effects on sound-evoked responses in inferior colliculus. J.Neurophysiol. 2006, 96:2177-2188.
22. Hurley L.M., Pollak G.D. Serotonin differentially modulates responses to tones and frequency-modulated sweeps in the inferior colliculus. J.Neurosci. 1999, 19:8071-8082.
23. Hurley L.M., Thompson A.M. Serotonergic innervation of the auditory brainstem of the Mexican free-tailed bat, Tadarida brasiliensis. J.Comp. Neurol. 2001, 435:78-88.
24. Hurley L.M., Pollak G.D. Serotonin effects on frequency tuning of inferior colliculus neurons. J.Neurophysiol. 2001, 85:828-842.
25. Hurley L.M., Pollak G.D. Serotonin modulates responses to species-specific vocalizations in the inferior colliculus. J.Comp. Physiol. A Neuroethol Sens Neural Behav. Physiol. 2005, 191:535-546.
26. Hurley L.M., Hall I.C. Context-dependent modulation of auditory processing by serotonin. Hear. Res. 2011, 279:74-84.
27. Hurley L.M., Sullivan M.R. From behavioral context to receptors: serotonergic modulatory pathways in the IC. Front. Neural Circuits 2012, 6:58.
28. Hurley L.M., Thompson A.M., Pollak G.D. Serotonin in the inferior colliculus. Hear. Res. 2002, 168:1-11.
29. Kanwal J.S., Matsumura S., Ohlemiller K., Suga N. Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. J.Acoust. Soc. Am. 1994, 96:1229-1254.
30. Klug A., Bauer E.E., Hanson J.T., Hurley L., Meitzen J., Pollak G.D. Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition. J.Neurophysiol. 2002, 88:1941-1954.
31. Koch U., Grothe B. GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J.Neurophysiol. 1998, 80:71-82.
32. Kuo R.I., Wu G.K. Generation of direction selectivity in the auditory system. Neuron 2012, 73:1016-1027.
33. LeBeau F.E., Malmierca M.S., Rees A. Iontophoresis invivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J.Neurosci. 2001, 21:7303-7312.
34. Li N., Gittelman J.X., Pollak G.D. Intracellular recordings reveal novel features of neurons that code interaural intensity disparities in the inferior colliculus. J.Neurosci. 2010, 30:14573-14584.
35. Liberman A.M., Mattingly I.G. Aspecialization for speech perception. Science 1989, 243:489-494.
36. Loftus W.C., Bishop D.C., Oliver D.L. Differential patterns of inputs create functional zones in central nucleus of inferior colliculus. J.Neurosci. 2010, 30:13396-13408.
37. Marler P. Bird calls: their potential for behavioral neurobiology. Ann. N. Y Acad. Sci. 2004, 1016:31-44.
38. Mayko Z.M., Roberts P.D., Portfors C.V. Inhibition shapes selectivity to vocalizations in the inferior colliculus of awake mice. Front. Neural Circuits 2012, 6:73.
39. Pollak G.D. Discriminating among complex signals: the roles of inhibition for creating response selectivities. J.Comp. Physiol. A Neuroethol Sens Neural Behav. Physiol. 2011, 197:625-640.
40. Pollak G.D., Gittelman J.X., Li N., Xie R. Inhibitory projections from the ventral nucleus of the lateral lemniscus and superior paraolivary nucleus create directional selectivity of frequency modulations in the inferior colliculus: a comparison of bats with other mammals. Hear. Res. 2011, 273:134-144.
41. Pollak G.D., Xie R., Gittelman J.X., Andoni S., Li N. The dominance of inhibition in the inferior colliculus. Hear. Res. 2011, 274:27-39.
42. Portfors C.V. Combination sensitivity and processing of communication calls in the inferior colliculus of the Moustached Bat Pteronotus parnellii. An Acad. Bras Cienc 2004, 76:253-257.
43. Priebe N.J., Ferster D. Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 2005, 45:133-145.
44. Razak K.A., Fuzessery Z.M. Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat. J.Neurophysiol. 2006, 96:1303-1319.
45. Razak K.A., Fuzessery Z.M. GABA shapes selectivity for the rate and direction of frequency modulated sweeps in the auditory cortex. J.Neurophysiol. 2009, 102:1366-1378.
46. Schneider D.M., Woolley S.M. Discrimination of communication vocalizations by single neurons and groups of neurons in the auditory midbrain. J.Neurophysiol. 2010, 103:3248-3265.
47. Sivaramakrishnan S., Oliver D.L. Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. J.Neurosci. 2001, 21:2861-2877.
48. Suga N. Feature extraction in the auditory system of bats. Basic Mechanisms in Hearing 1973, 675-744. Academic Press, New York. A.R. Moller (Ed.).
49. Suga N., Schlegel P. Coding and processing in the auditory systems of FM-signal-producing bats. J.Acoust. Soc. Am. 1973, 54:174-190.
50. Suta D., Kvasnak E., Popelar J., Syka J. Representation of species-specific vocalizations in the inferior colliculus of the guinea pig. J.Neurophysiol. 2003, 90:3794-3808.
51. Tan M.L., Theeuwes H.P., Feenstra L., Borst J.G. Membrane properties and firing patterns of inferior colliculus neurons: an invivo patch-clamp study in rodents. J.Neurophysiol. 2007, 98:443-453.
52. Thompson G.C., Thompson A.M., Garrett K.M., Britton B.H. Serotonin and serotonin receptors in the central auditory system. Otolaryngol. Head Neck Surg. 1994, 110:93-102.
53. Williams A.J., Fuzessery Z.M. Multiple mechanisms shape FM sweep rate selectivity: complementary or redundant?. Front. Neural Circuits 2012, 6:54.
54. Woolley S.M., Fremouw T.E., Hsu A., Theunissen F.E. Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nat. Neurosci. 2005, 8:1371-1379.
55. Xie R., Meitzen J., Pollak G.D. Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei. J.Neurophysiol. 2005, 94:4019-4037.
56. Xie R., Gittelman J.X., Pollak G.D. Rethinking tuning: invivo whole-cell recordings of the inferior colliculus in awake bats. J.Neurosci. 2007, 27:9469-9481.
57. Xie R., Gittelman J.X., Li N., Pollak G.D. Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus. Neuroscience 2008, 154:245-256.
58. Yang L., Pollak G.D. Binaural inhibition in the dorsal nucleus of the lateral lemniscus of the mustache bat affects responses for multiple signals. Auditory Neurosci. 1994, 1:1-17.
59. Yang L., Pollak G.D. Features of ipsilaterally evoked inhibition in the dorsal nucleus of the lateral lemniscus. Hear. Res. 1998, 122:125-141.
60. Yang L., Pollak G.D., Resler C. GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J.Neurophysiol. 1992, 68:1760-1774.
61. Ye C.Q., Poo M.M., Dan Y., Zhang X.H. Synaptic mechanisms of direction selectivity in primary auditory cortex. J. Neurosci. 2010, 1861-1868.
62. Yue Q., Casseday J.H., Covey E. Response properties and location of neurons selective for sinusoidal frequency modulations in the inferior colliculus of the big brown bat. J.Neurophysiol. 2007, 98:1364-1373.
63. Zhang L.I., Tan A.Y., Schreiner C.E., Merzenich M.M. Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 2003, 424:201-205.