Abstract
The inferior colliculus and auditory cortex of the pallid bat contain a large percentage of neurons that are highly selective for the direction and rate of the downward frequency modulated (FM) sweep of the bat’s echolocation pulse. Approximately 25% of neurons tuned to the echolocation pulse respond exclusively to downward FM sweeps. This review focuses on the finding that this selectivity is generated by multiple mechanisms that may act alone or in concert. In the inferior colliculus, selectivity for sweep rate is shaped by at least three mechanisms: shortpass or bandpass tuning for signal duration, delayed high-frequency inhibition that prevents responses to slow sweep rates, and asymmetrical facilitation that occurs only when two tones are presented at appropriate delays. When acting alone, the three mechanisms can produce essentially identical rate selectivity. Direction selectivity can be produced by two mechanisms: an early low-frequency inhibition that prevents responses to upward sweeps, and the same asymmetrical two-tone inhibition that shapes rate tuning. All mechanisms except duration tuning are also present in the auditory cortex. Discussion centers on whether these mechanisms are redundant or complementary.
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Abbreviations
- FM:
-
frequency modulated
- TTF:
-
two-tone facilitation
- DSI:
-
direction selectivity index
References
Andoni S, Li N, Pollak GD (2007) Spectrotemporal receptive fields in the inferior colliculus revealing selectivity for spectral motion in conspecific vocalizations. J Neurosci 27:4882–4893
Barber JR, Razak KA, Fuzessery ZM (2003) Can two streams of information be processed simultaneously? Evidence from the gleaning bat Antrozous pallidus. J Comp Physiol 189:843–855
Barlow HB, Levick WR (1964) The mechanisms of directionally selective units in rabbit’s retina. J Physiol (Lond) 178:477–504
Britt S, Starr A (1976) Synaptic events and discharge patterns of cochlear nucleus II. Frequency modulated tones. J Neurophysiol 39:179–194
Brown P (1976) Vocal communication in the pallid bat, Antrozous pallidus. Z Tierpsychol 41:34–54
Casseday JH, Covey E, Grothe B (1997) Neural selectivity and tuning for sinusoidal frequency modulations in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77:1595–1607
Covey E, Casseday JH (1999) Timing in the auditory system of the bat. Annu Rev Physiol 61:457–476
Fishbach A, Yeshurun Y, Nelken I (2003) Neural model for physiological responses to frequency and amplitude transitions uncovers topographic order in auditory cortex. J Neurophysiol 90:3663–3678
Fuzessery ZM (1994) Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus. J Neurophysiol 72:1061–1079
Fuzessery ZM (1997) Acute sensitivity to interaural time differences in the inferior colliculus of a bat that relies on passive sound localization. Hear Res 109:46–62
Fuzessery ZM, Hall JC (1999) Sound duration selectivity in the pallid bat inferior colliculus. Hear Res 137:137–154
Fuzessery ZM, Buttenhoff P, Andrews B, Kennedy JM (1993) Passive sound localization of prey by the pallid bat (Antrozous p pallidus). J Comp Physiol 171:767–777
Fuzessery ZM, Richardson MD, Coburn MS (2006) Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the inferior colliculus of the pallid bat. J Neurophysiol 96:1320–1336
Gordon M, O’Neill WE (1998) Temporal processing across frequency channels by FM selective auditory neurons can account for FM rate selectivity. Hear Res 122:97–108
Gulledge AT, Kampa BM, Stuart GJ (2005) Synaptic integration in dendritic trees. J Neurobiol 64:75–90
Heil P, Langer G, Scheich H (1992) Processing of frequency-modulated stimuli in the chick AC analogue: evidence for topographic representations and possible mechanisms of rate and direction sensitivity. J Comp Physiol 171:583–600
Livingstone MS (1998) Mechanisms of direction selectivity in macaque V1. Neuron 20:509–526
Phillips DP, Mendelson JR, Cynader MS, Douglas RM (1985) Responses of single neurons in cat auditory cortex to time-varying stimulus: frequency-modulated tones of narrow excursion. Exp Brain Res 58:479–492
Rall W (1959) Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol 1:491–527
Razak KA, Fuzessery ZM (2002) Functional organization of the pallid bat auditory cortex: emphasis on binaural organization. J Neurophysiol 87:72–86
Razak KA, Fuzessery ZM (2006) Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat. J Neurophysiol 96:1303–1319
Razak KA, Fuzessery ZM (2008) Facilitatory mechanisms underlying selectivity for the direction and rate of frequency modulated sweeps in the auditory cortex. J Neurosci 28(39):9806–9816
Razak KA, Fuzessery ZM (2009) GABA shapes selectivity for the rate and direction of frequency-modulated sweeps in the audiutory cortex. J Neurophysiol 102:1366–1378
Razak KA, Shen W, Zumsteg T, Fuzessery ZM (2007) Parallel thalamocortical pathways for echolocation and passive sound localization in a gleaning bat, Antrozous pallidus. J Comp Neurol 500:322–338
Reid RC, Soodak RE, Shapley RM (1991) Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. J Neurophysiol 66:505–529
Rubsamen R, Neuweiler G, Sripathi K (1988) Comparative collicular tonotopy in two bat species adapted to movement detection, Hipposideros speoris and Megaderma lyra. J Comp Physiol 163:271–285
Sanchez JT, Gans D, Wenstrup JJ (2008) Glycinergic “inhibition” mediates selective excitatory responses to combinations of sounds. J Neurosci 28:80–90
Segev I (1992) Single neurone models: oversimple, complex and reduced. Trends Neurosci 15:414–421
Shannon-Hartman S, Wong D, Maekawa M (1992) Processing of pure-tone and FM stimuli in the auditory cortex of the FM bat, Myotis lucifugus. Hear Res 61:179–188
Sillito AM (1977) Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in cat’s visual cortex. J Physiol (Lond) 271:699–720
Softky W (1994) Sub-millisecond coincidence detection in active dendritic trees. Neuroscience 58:13–41
Suga N (1965) Functional properties of auditory neurones in the cortex of echo-locating bats. J Physiol 181:671–700
Voytenko SV, Galazyuk AV (2007) Intracellular recording reveals temporal integration in inferior colliculus neurons in awake bats. J Neurophysiol 97:1368–1378
Zhang LI, Tan AY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424:201–205
Acknowledgments
This review is dedicated to Gerhard Neuweiler. We thank Terri Zumsteg for her assistance with this manuscript. Research was supported by NIH NIDCD Grant DC05202 to ZMF.
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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 197, 615–623 (2011). https://doi.org/10.1007/s00359-010-0554-0
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DOI: https://doi.org/10.1007/s00359-010-0554-0