Midbrain auditory neurons integrate excitation and inhibition to generate duration selectivity: An in vivo whole-cell patch study in anurans

Journal of Neuroscience

Volumn 28, Issue 21, 2008, Pages 5481-5493

  Leary, Christopher J ^a   Edwards, Christofer J ^a   Rose, Gary J ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Acoustic; Auditory; In vivo; Inferior colliculus; Intracellular; Patch clamp; Temporal coding

Indexed keywords

ACOUSTIC NERVE FIBER; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; DOSE TIME EFFECT RELATION; FROG; IN VIVO STUDY; LATENT PERIOD; MESENCEPHALON; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; SEMICIRCULAR CANAL; STIMULUS RESPONSE; ACTION POTENTIAL; ANIMAL; AUDITORY STIMULATION; CYTOLOGY; ELECTROSTIMULATION; FROGS AND TOADS; INHIBITORY POSTSYNAPTIC POTENTIAL; METHODOLOGY; NERVE CELL INHIBITION; PATCH CLAMP; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; SENSORY NERVE CELL; TIME;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; ANURA; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; INHIBITORY POSTSYNAPTIC POTENTIALS; MESENCEPHALON; NEURAL INHIBITION; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; TIME FACTORS;

EID: 45849144389     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5041-07.2008     Document Type: Article

References (33)

1. Alder TB, Rose GJ (2000) Integration and recovery processes contribute to the temporal selectivity of neurons in the northern leopard frog, Rana pipiens. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 186:923-937.
2. Brenowitz EA, Rose GJ, Alder T (2001) The neuroethology of acoustic communication in Pacific treefrogs. In: Anuran communication (Ryan MJ, ed), pp 145-155. Washington, DC: Smithsonian Institution.
3. Casseday JH, Ehrlich D, Covey E (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264:847-850.
4. Casseday JH, Erlich D, Covey E (2000) Neural measurement of sound duration: control by excitatory-inhibitory interactions in the inferior colliculus. J Neurophysiol 84:1475-1487.
5. Casseday JH, Fremouw T, Covey E (2002) The inferior colliculus: a hub for the central auditory system. In: Integrative functions in the mammalian auditory pathway (Oertel D, Fay RR, Popper AN, eds), pp 238-318. New York: Springer.
6. Covey E, Kauer JA, Casseday JH (1996) Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic current in the inferior colliculus of awake bats. J Neurosci 16:3009-3018.
7. Edwards CJ, Rose GJ (2003) Interval-integration underlies amplitude modulation band-suppression selectivity in the anuran midbrain. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:907-914.
8. Edwards CJ, Alder TB, Rose GJ (2002) Auditory midbrain neurons that count. Nat Neurosci 5:934-936.
9. Edwards CJ, Leary CJ, Rose GJ (2007) Counting on inhibition and rate-dependent excitation in the auditory system. J Neurosci 27:13384-13392.
10. Ehrlich D, Casseday JH, Covey E (1997) Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77:2360-2372.
11. Faure PA, Fremouw T, Casseday JH, Covey E (2003) Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J Neurosci 23:3052-3065.
12. Fuzessery ZM, Hall JC (1999) Sound duration selectivity in the pallid bat inferior colliculus. Hear Res 137:137-154.
13. Gerhardt HC (1982) Sound pattern recognition in some North American treefrogs (Anura: Hylidae): implications for mate choice. Am Zool 22:581-595.
14. Gerhardt HC (1988) Acoustic properties used in call recognition by frogs and toads. In: The evolution of the amphibian auditory system (Fritszch B, Wilczynski W, Ryan MJ, Hetherington TE, Walkowiak W, eds), pp 275-294. New York: Wiley.
15. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. Chicago: University of Chicago.
16. Gooler DM, Feng AS (1992) Temporal coding in the frog midbrain: the influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli. J Neurophysiol 67:1-22.
17. Hall JC (1999) GABAergic inhibition shapes frequency tuning and modifies response properties in the midbrain of the leopard frog. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 185:479-491.
18. Hollis DM, Boyd SK (2004) Distribution of GABA-like immunoreactive cell bodies in the brains of two amphibians, Rana catesbeiana and Xenopus laevis. Brain Behav Evol 65:127-142.
19. Jen P H-S, Wu CH (2005) The role of GABAergic inhibition in shaping the response size and duration selectivity of bat inferior collicular neurons to sound pulses in rapid sequences. Hear Res 202:222-234.
20. Lehiste I, Olive JP, Streeter LA (1976) Role of duration in disambiguating syntactically ambiguous sentences. J Acoust Soc Am 60:1199-1202.
21. Masterton RB (1992) Role of the central auditory system in hearing: the new direction. Trends Neurosci 15:280-285.
22. Mora EC, Kössl M (2004) Ambiguities in sound-duration selectivity by neurons in the inferior colliculus of the bat Molossus molossus from Cuba. J Neurophysiol 91:2215-2226.
23. Narins PM, Capranica RR (1980) Neural adaptations for processing the two-note call of the Puerto Rican treefrog, Eleutherodactylus coqui. Brain Behav Evol 17:48-66.
24. Pinheiro AD, Wu M, Jen PH (1991) Encoding repetition rate and duration in the inferior colliculus of the big brown bat Eptesicus fuscus. J Comp Physiol 169:69-85.
25. Potter HD (1965) Patterns of acoustically-evoked dischanges of neurons in the mesencephalon of the bullfrog. J Neurophysiol 28:1155-1184.
26. Rose G, Capranica RR (1983) Temporal selectivity in the central auditory system of the leopard frog Rana pipiens. Science 219:1087-1089.
27. Rose GJ, Brenowitz EA (1997) Plasticity of aggressive thresholds in Hyla regilla: discrete accommodation to encounter calls. Anim Behav 53:353-361.
28. Rose GJ, Brenowitz EA (2002) Pacific treefrogs use temporal integration to differentiate advertisement from encounter calls. Anim Behav 63:1183-1190.
29. Rose GJ, Fortune ES (1996) New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci Res 26:89-94.
30. Rose GJ, Gooler DM (2007) Function of the anuran central auditory system. In: Hearing and sound communication in amphibians. Springer handbook of auditory research (Feng AS, Narins PM, Fay RH, Popper AH, eds), pp 250-290. New York: Springer.
31. Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303-304.
32. Suga N (1988) Auditory neuroethology and speech processing: complex-sound processing by combination-sensitive neurons. In: Auditory function: neurobiological bases of hearing (Edelman GM, Gall WE, Cowan WM, eds), pp 679-720. New York: Wiley.
33. Wells KD, Schwartz JJ (2007) The behavioral ecology of anuran communication. In: Hearing and sound communication in amphibians. Springer handbook of auditory ressearch (Feng AS, Narins PM, Fay RH, Popper AH, eds), pp 44-86. New York: Springer.