A mechanistic understanding of the role of feedforward inhibition in the mammalian sound localization circuitry

Neuron

Volumn 78, Issue 5, 2013, Pages 923-935

  Roberts, MichaelT ^a   Seeman, StephanieC ^a   Golding, NaceL ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SHAKER POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; AUDITORY SYSTEM FUNCTION; AUDITORY SYSTEM PARAMETERS; BINAURAL HEARING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GERBIL; HYPERPOLARIZATION; INTEGRATION; NERVE CELL; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL STIMULATION; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SOUND DETECTION; SUPERIOR OLIVARY NUCLEUS;

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; AUDITORY PATHWAYS; BIOPHYSICAL PROCESSES; BIOPHYSICS; ELAPID VENOMS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FUNCTIONAL LATERALITY; GERBILLINAE; NERVE NET; NEURAL INHIBITION; NEURONS; NEUROTOXINS; OLIVARY NUCLEUS; POTASSIUM CHANNEL BLOCKERS; SOUND LOCALIZATION;

EID: 84878864813     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.04.022     Document Type: Article

References (74)

1. Allen P.D., Ison J.R. Kcna1 gene deletion lowers the behavioral sensitivity of mice to small changes in sound location and increases asynchronous brainstem auditory evoked potentials but does not affect hearing thresholds. J.Neurosci. 2012, 32:2538-2543.
2. Bal R., Oertel D. Potassium currents in octopus cells of the mammalian cochlear nucleus. J.Neurophysiol. 2001, 86:2299-2311.
3. Banke T.G., McBain C.J. GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J.Neurosci. 2006, 26:11720-11725.
4. Borst J.G.G., Soria van Hoeve J. The calyx of held synapse: from model synapse to auditory relay. Annu. Rev. Physiol. 2012, 74:199-224.
5. Brand A., Behrend O., Marquardt T., McAlpine D., Grothe B. Precise inhibition is essential for microsecond interaural time difference coding. Nature 2002, 417:543-547.
6. Brew H.M., Hallows J.L., Tempel B.L. Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1.1. J.Physiol. 2003, 548:1-20.
7. Brownell W.E. Organization of the cat trapezoid body and the discharge characteristics of its fibers. Brain Res. 1975, 94:413-433.
8. Cant N.B., Hyson R.L. Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hear. Res. 1992, 58:26-34.
9. Chirila F.V., Rowland K.C., Thompson J.M., Spirou G.A. Development of gerbil medial superior olive: integration of temporally delayed excitation and inhibition at physiological temperature. J.Physiol. 2007, 584:167-190.
10. Choquet D., Korn H. Mechanism of 4-aminopyridine action on voltage-gated potassium channels in lymphocytes. J.Gen. Physiol. 1992, 99:217-240.
11. Clark G.M. The ultrastructure of nerve endings in the medial superior olive of the cat. Brain Res. 1969, 14:293-305.
12. Cobb S.R., Buhl E.H., Halasy K., Paulsen O., Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 1995, 378:75-78.
13. Couchman K., Grothe B., Felmy F. Medial superior olivary neurons receive surprisingly few excitatory and inhibitory inputs with balanced strength and short-term dynamics. J.Neurosci. 2010, 30:17111-17121.
14. Day M.L., Semple M.N. Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays. J.Neurophysiol. 2011, 106:1985-1999.
15. Dodson P.D., Barker M.C., Forsythe I.D. Two heteromeric Kv1 potassium channels differentially regulate action potential firing. J.Neurosci. 2002, 22:6953-6961.
16. Economo M.N., Fernandez F.R., White J.A. Dynamic clamp: alteration of response properties and creation of virtual realities in neurophysiology. J.Neurosci. 2010, 30:2407-2413.
17. Fischl M.J., Combs T.D., Klug A., Grothe B., Burger R.M. Modulation of synaptic input by GABAB receptors improves coincidence detection for computation of sound location. J.Physiol. 2012, 590:3047-3066.
18. Funabiki K., Koyano K., Ohmori H. The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick. J.Physiol. 1998, 508:851-869.
19. Gabernet L., Jadhav S.P., Feldman D.E., Carandini M., Scanziani M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 2005, 48:315-327.
20. Gittelman J.X., Tempel B.L. Kv1.1-containing channels are critical for temporal precision during spike initiation. J.Neurophysiol. 2006, 96:1203-1214.
21. Grothe B. Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. J.Neurophysiol. 1994, 71:706-721.
22. Grothe B. New roles for synaptic inhibition in sound localization. Nat. Rev. Neurosci. 2003, 4:540-550.
23. Grothe B., Park T.J. Sensitivity to interaural time differences in the medial superior olive of a small mammal, the Mexican free-tailed bat. J.Neurosci. 1998, 18:6608-6622.
24. Grothe B., Sanes D.H. Bilateral inhibition by glycinergic afferents in the medial superior olive. J.Neurophysiol. 1993, 69:1192-1196.
25. Grothe B., Sanes D.H. Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: an invitro study. J.Neurosci. 1994, 14:1701-1709.
26. Hille B. Ion Channels of Excitable Membranes 2001, Sinauer, Sunderland, MA.
27. Howard M.A., Rubel E.W. Dynamic spike thresholds during synaptic integration preserve and enhance temporal response properties in the avian cochlear nucleus. J.Neurosci. 2010, 30:12063-12074.
28. Howard M.A., Burger R.M., Rubel E.W. A developmental switch to GABAergic inhibition dependent on increases in Kv1-type K+ currents. J.Neurosci. 2007, 27:2112-2123.
29. Hyson R.L., Reyes A.D., Rubel E.W. A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick. Brain Res. 1995, 677:117-126.
30. Ingham N.J., McAlpine D. GABAergic inhibition controls neural gain in inferior colliculus neurons sensitive to interaural time differences. J.Neurosci. 2005, 25:6187-6198.
31. Jercog P.E., Svirskis G., Kotak V.C., Sanes D.H., Rinzel J. Asymmetric excitatory synaptic dynamics underlie interaural time difference processing in the auditory system. PLoS Biol. 2010, 8:e1000406.
32. Johnson D.H. The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J.Acoust. Soc. Am. 1980, 68:1115-1122.
33. Johnston J., Forsythe I.D., Kopp-Scheinpflug C. Going native: voltage-gated potassium channels controlling neuronal excitability. J.Physiol. 2010, 588:3187-3200.
34. Joris P., Yin T.C.T. A matter of time: internal delays in binaural processing. Trends Neurosci. 2007, 30:70-78.
35. Joris P.X., Carney L.H., Smith P.H., Yin T.C. Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J.Neurophysiol. 1994, 71:1022-1036.
36. Joris P.X., Van de Sande B., Louage D.H., van der Heijden M. Binaural and cochlear disparities. Proc. Natl. Acad. Sci. USA 2006, 103:12917-12922.
37. Kapfer C., Seidl A.H., Schweizer H., Grothe B. Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat. Neurosci. 2002, 5:247-253.
38. Khurana S., Remme M.W.H., Rinzel J., Golding N.L. Dynamic interaction of Ih and IK-LVA during trains of synaptic potentials in principal neurons of the medial superior olive. J.Neurosci. 2011, 31:8936-8947.
39. Kopp-Scheinpflug C., Fuchs K., Lippe W.R., Tempel B.L., Rübsamen R. Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study invivo. J.Neurosci. 2003, 23:9199-9207.
40. Kopp-Scheinpflug C., Steinert J.R., Forsythe I.D. Modulation and control of synaptic transmission across the MNTB. Hear. Res. 2011, 279:22-31.
41. Kuenzel T., Borst J.G.G., van der Heijden M. Factors controlling the input-output relationship of spherical bushy cells in the gerbil cochlear nucleus. J.Neurosci. 2011, 31:4260-4273.
42. Kuo S.P., Bradley L.A., Trussell L.O. Heterogeneous kinetics and pharmacology of synaptic inhibition in the chick auditory brainstem. J.Neurosci. 2009, 29:9625-9634.
43. Kuwabara N., Zook J.M. Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. J.Comp. Neurol. 1992, 324:522-538.
44. Leão R.M., Kushmerick C., Pinaud R., Renden R., Li G.-L., Taschenberger H., Spirou G., Levinson S.R., von Gersdorff H. Presynaptic Na+ channels: locus, development, and recovery from inactivation at a high-fidelity synapse. J.Neurosci. 2005, 25:3724-3738.
45. Leibold C. Influence of inhibitory synaptic kinetics on the interaural time difference sensitivity in a linear model of binaural coincidence detection. J.Acoust. Soc. Am. 2010, 127:931-942.
46. Lorteije J.A.M., Rusu S.I., Kushmerick C., Borst J.G.G. Reliability and precision of the mouse calyx of Held synapse. J.Neurosci. 2009, 29:13770-13784.
47. Lu T., Trussell L.O. Inhibitory transmission mediated by asynchronous transmitter release. Neuron 2000, 26:683-694.
48. Magnusson A.K., Kapfer C., Grothe B., Koch U. Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset. J.Physiol. 2005, 568:497-512.
49. Maki K., Furukawa S. Acoustical cues for sound localization by the Mongolian gerbil, Meriones unguiculatus. J.Acoust. Soc. Am. 2005, 118:872-886.
50. Mathews P.J., Jercog P.E., Rinzel J., Scott L.L., Golding N.L. Control of submillisecond synaptic timing in binaural coincidence detectors by K(v)1 channels. Nat. Neurosci. 2010, 13:601-609.
51. Mc Laughlin M., van der Heijden M., Joris P.X. How secure is invivo synaptic transmission at the calyx of Held?. J.Neurosci. 2008, 28:10206-10219.
52. Oertel D., Shatadal S., Cao X.-J. In the ventral cochlear nucleus Kv1.1 and subunits of HCN1 are colocalized at surfaces of neurons that havelow-voltage-activated and hyperpolarization-activated conductances. Neuroscience 2008, 154:77-86.
53. Pecka M., Brand A., Behrend O., Grothe B. Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J.Neurosci. 2008, 28:6914-6925.
54. Pouille F., Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293:1159-1163.
55. Prinz A.A., Abbott L.F., Marder E. The dynamic clamp comes of age. Trends Neurosci. 2004, 27:218-224.
56. Rothman J.S., Manis P.B. Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. J.Neurophysiol. 2003, 89:3083-3096.
57. Scott L.L., Mathews P.J., Golding N.L. Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. J.Neurosci. 2005, 25:7887-7895.
58. Scott L.L., Mathews P.J., Golding N.L. Perisomatic voltage-gated sodium channels actively maintain linear synaptic integration in principal neurons of the medial superior olive. J.Neurosci. 2010, 30:2039-2050.
59. Seidl A.H., Rubel E.W., Harris D.M. Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J.Neurosci. 2010, 30:70-80.
60. Shamma S.A., Shen N.M., Gopalaswamy P. Stereausis: binaural processing without neural delays. J.Acoust. Soc. Am. 1989, 86:989-1006.
61. Sheng M., Tsaur M.L., Jan Y.N., Jan L.Y. Contrasting subcellular localization of the Kv1.2 K+ channel subunit in different neurons of rat brain. J.Neurosci. 1994, 14:2408-2417.
62. Spirou G.A., Rowland K.C., Berrebi A.S. Ultrastructure of neurons and large synaptic terminals in the lateral nucleus of the trapezoid body of the cat. J.Comp. Neurol. 1998, 398:257-272.
63. Stephens G.J., Garratt J.C., Robertson B., Owen D.G. On the mechanism of 4-aminopyridine action on the cloned mouse brain potassium channel mKv1.1. J.Physiol. 1994, 477:187-196.
64. Stokes C.C.A., Isaacson J.S. From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex. Neuron 2010, 67:452-465.
65. Svirskis G., Kotak V., Sanes D.H., Rinzel J. Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. J.Neurosci. 2002, 22:11019-11025.
66. Svirskis G., Kotak V., Sanes D.H., Rinzel J. Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. J.Neurophysiol. 2004, 91:2465-2473.
67. Tang Z.-Q., Dinh E.H., Shi W., Lu Y. Ambient GABA-activated tonic inhibition sharpens auditory coincidence detection via a depolarizing shunting mechanism. J.Neurosci. 2011, 31:6121-6131.
68. Trimmer J.S., Rhodes K.J. Localization of voltage-gated ion channels in mammalian brain. Annu. Rev. Physiol. 2004, 66:477-519.
69. van der Heijden M., Lorteije J.A.M., PlauŠka A., Roberts M.T., Golding N.L., Borst J.G.G. Directional hearing by linear summation of binaural inputs at the medial superior olive. Neuron 2013, 78:936-948. this issue.
70. Vida I., Bartos M., Jonas P. Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 2006, 49:107-117.
71. Wang H., Kunkel D.D., Schwartzkroin P.A., Tempel B.L. Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J.Neurosci. 1994, 14:4588-4599.
72. Yang L., Monsivais P., Rubel E.W. The superior olivary nucleus and its influence on nucleus laminaris: a source of inhibitory feedback for coincidence detection in the avian auditory brainstem. J.Neurosci. 1999, 19:2313-2325.
73. Yin T.C., Chan J.C. Interaural time sensitivity in medial superior olive of cat. J.Neurophysiol. 1990, 64:465-488.
74. Zhou Y., Carney L.H., Colburn H.S. A model for interaural time difference sensitivity in the medial superior olive: interaction of excitatory and inhibitory synaptic inputs, channel dynamics, and cellular morphology. J.Neurosci. 2005, 25:3046-3058.