Abstract
Neural adaptation, a reduction in the response to a maintained stimulus, is an important mechanism for detecting stimulus change. Contributing to change detection is the fact that adaptation is often stimulus specific: adaptation to a particular stimulus reduces excitability to a specific subset of stimuli, while the ability to respond to other stimuli is unaffected. Phasic cells (e.g., cells responding to stimulus onset) are good candidates for detecting the most rapid changes in natural auditory scenes, as they exhibit fast and complete adaptation to an initial stimulus presentation. We made recordings of single phasic auditory units in the frog midbrain to determine if adaptation was specific to stimulus frequency and ear of input. In response to an instantaneous frequency step in a tone, 28 % of phasic cells exhibited frequency specific adaptation based on a relative frequency change (delta-f = ±16 %). Frequency specific adaptation was not limited to frequency steps, however, as adaptation was also overcome during continuous frequency modulated stimuli and in response to spectral transients interrupting tones. The results suggest that adaptation is separated for peripheral (e.g., frequency) channels. This was tested directly using dichotic stimuli. In 45 % of binaural phasic units, adaptation was ear specific: adaptation to stimulation of one ear did not affect responses to stimulation of the other ear. Thus, adaptation exhibited specificity for stimulus frequency and lateralization at the level of the midbrain. This mechanism could be employed to detect rapid stimulus change within and between sound sources in complex acoustic environments.
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Abbreviations
- BF:
-
Best frequency
- CRW:
-
Change response window
- ESA:
-
Ear specific adaptation
- ERB:
-
Equivalent rectangular bandwidth
- F1:
-
First frequency presented
- F2:
-
Second frequency presented
- FM:
-
Frequency modulation
- FSA:
-
Frequency specific adaptation
- MMN:
-
Mismatch negativity
- ORW:
-
Onset response window
- SSA:
-
Stimulus specific adaptation
References
Adrian ED, Zotterman Y (1926) The impulses produced by sensory nerve-endings: part II. The response of a single end-organ. J Physiol 61:151–171
Antunes FM, Nelken I, Covey E, Malmierca MS (2010) Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS One 5:e14071
Bass AH, Rose GJ, Pritz MB (2005) Auditory midbrain of fish, amphibians and reptiles: model systems for understanding auditory function. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 459–492
Bauerle P, von der BW, Kossl M, Gaese BH (2011) Stimulus-specific adaptation in the gerbil primary auditory thalamus is the result of a fast frequency-specific habituation and is regulated by the corticofugal system. J Neurosci 31:9708–9722
Bee MA, Micheyl C (2008) The cocktail party problem: what is it? How can it be solved? And why should animal behaviorists study it? J Comp Psychol 122:235–251
Bee MA, Micheyl C, Oxenham AJ, Klump GM (2010) Neural adaptation to tone sequences in the songbird forebrain: patterns, determinants, and relation to the build-up of auditory streaming. J Comp Physiol A 196:543–557
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Assoc. Inc., Sunderland
Bregman AS (1990) Auditory scene analysis: The perceptual organization of sound. MIT Press, Cambridge
Brimijoin WO, O’Neill WE (2005) On the prediction of sweep rate and directional selectivity for FM sounds from two-tone interactions in the inferior colliculus. Hear Res 210:63–79
Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197:705–722
Cai H, Carney LH, Colburn HS (1998a) A model for binaural response properties of inferior colliculus neurons. I. A model with interaural time difference-sensitive excitatory and inhibitory inputs. J Acoust Soc Am 103:475–493
Cai H, Carney LH, Colburn HS (1998b) A model for binaural response properties of inferior colliculus neurons. II. A model with interaural time difference-sensitive excitatory and inhibitory inputs and an adaptation mechanism. J Acoust Soc Am 103:494–506
Carlyon RP (2004) How the brain separates sounds. Trends Cogn Sci 8:465–471
Condon CD, Weinberger NM (1991) Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex. Behav Neurosci 105:416–430
Demany L, Semal C (2008) The role of memory in auditory perception. In: Yost WA, Popper AN, Fay RR (eds) Auditory perception of sound sources. Springer, New York, pp 77–113
Dong S, Clayton DF (2009) Habituation in songbirds. Neurobiol Learn Mem 92:183–188
Eggermont JJ (2000) Neural responses in primary auditory cortex mimic psychophysical, across-frequency-channel, gap-detection thresholds. J Neurophysiol 84:1453–1463
Ehret G, Capranica RR (1980) Masking patterns and filter characteristics of auditory-nerve fibers in the green treefrog (Hyla-cinerea). J Comp Physiol 141:1–12
Fay RR (2008) Sound source perception and stream segregation in nonhuman vertebrate animals. In: Yost WA, Popper AN, Fay RR (eds) Auditory perception of sound sources. Springer, New York, pp 307–323
Feng AS (1982) Quantitative analysis of intensity—rate and intensity—latency functions in peripheral auditory nerve fibers of northern leopard frogs (Rana p. pipiens). Hear Res 6:241–246
Feng AS, Lin WY (1994) Phase-locked response characteristics of single neurons in the frog “cochlear nucleus” to steady-state and sinusoidal-amplitude-modulated tones. J Neurophysiol 72:2209–2221
Feng AS, Ratnam R (2000) Neural basis of hearing in real-world situations. Annu Rev Psychol 51:699–725
Feng AS, Shofner WP (1981) Peripheral basis of sound localization in anurans. Acoustic properties of the frog’s ear. Hear Res 5:201–216
Feng AS, Lin WY, Sun L (1994) Detection of gaps in sinusoids by frog auditory nerve fibers: importance in AM coding. J Comp Physiol A 175:531–546
Feng AS, Arch VS, Yu ZL, Yu XJ, Xu ZM, Shen JX (2009) Neighbor-stranger discrimination in concave-eared torrent frogs, Odorrana tormota. Ethology 115:851–856
Formby C, Forrest TG (1991) Detection of silent temporal gaps in sinusoidal markers. J Acoust Soc Am 89:830–837
Fuzessery ZM (1988) Frequency tuning in the anuran central auditory system. In: Fritzch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 253–273
Fuzessery ZM, Feng AS (1982) Frequency-selectivity in the anuran auditory midbrain—single unit responses to single and multiple tone stimulation. J Comp Physiol 146:471–484
Fuzessery ZM, Feng AS (1983) Frequency selectivity in the anuran medulla: Excitatory and inhibitory tuning properties of single neurons in the dorsal medullary and superior olivary nuclei. J Comp Physiol 150:107–119
Glagow M, Ewert JP (1997) Dopaminergic modulation of visual responses in toads. II. Influences of apomorphine on retinal ganglion cells and tectal cells. J Comp Physiol A 180:11–18
Goense JB, Feng AS (2012) Effects of noise bandwidth and amplitude modulation on masking in frog auditory midbrain neurons. PLoS ONE 7:e31589
Gooler DM, Feng AS (1992) Temporal coding in the frog auditory midbrain: the influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli. J Neurophysiol 67:1–22
Green DM (1988) Profile analysis: auditory intensity discrimination. Oxford University Press, Oxford
Green DM, Forrest TG (1989) Temporal gaps in noise and sinusoids. J Acoust Soc Am 86:961–970
Grose JH, Hall JW III, Buss E, Hatch D (2001) Gap detection for similar and dissimilar gap markers. J Acoust Soc Am 109:1587–1595
Hall JC, Feng AS (1991) Temporal processing in the dorsal medullary nucleus of the Northern leopard frog (Rana pipiens pipiens). J Neurophysiol 66:955–973
Hall JW, Haggard MP, Fernandes MA (1984) Detection in noise by spectro-temporal pattern analysis. J Acoust Soc Am 76:50–56
Hartmann WH (1998) Signals, sound, and sensation. AIP Press, New York
Heinz MG, Goldstein MH, Formby C (1996) Temporal gap detection thresholds in sinusoidal markers simulated with a multi-channel, multi-resolution model of the auditory periphery. Aud Neurosci 3:35–56
Hemmi JM, Merkle T (2009) High stimulus specificity characterizes anti-predator habituation under natural conditions. Proc R Soc B 276:4381–4388
Ingham NJ, McAlpine D (2004) Spike-frequency adaptation in the inferior colliculus. J Neurophysiol 91:632–645
Joermann G (1988) Masked thresholds of auditory midbrain neurons in the frog Rana ridibunda. Hear Res 35:191–199
Krebs JR (1976) Habituation and song repertoires in great tit. Behav Ecol Sociobiol 1:215–227
Larson KA (2004) Advertisement call complexity in northern leopard frogs, Rana pipiens. Copeia 3:676–682
Liberman AM, Delattre P, Cooper FS (1952) The role of selected stimulus-variables in the perception of the unvoiced stop consonants. Am J Psychol 65:497–516
Liberman AM, Harris KS, Hoffman HS, Griffith BC (1957) The discrimination of speech sounds within and across phoneme boundaries. J Exp Psychol 54:358–368
Liberman AM, Harris KS, Kinney JA, Lane H (1961) The discrimination of relative onset-time of the components of certain speech and nonspeech patterns. J Exp Psychol 61:379–388
Liff H (1969) Responses from single auditory units in the eighth nerve of the Leopard frog. J Acoust Soc Am 45:512–513
Lumani A, Zhang H (2010) Responses of neurons in the rat’s dorsal cortex of the inferior colliculus to monaural tone bursts. Brain Res 1351:115–129
Malmierca MS, Cristaudo S, Perez-Gonzalez D, Covey E (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29:5483–5493
Malone BJ, Semple MN (2001) Effects of auditory stimulus context on the representation of frequency in the gerbil inferior colliculus. J Neurophysiol 86:1113–1130
Malone BJ, Scott BH, Semple MN (2002) Context-dependent adaptive coding of interaural phase disparity in the auditory cortex of awake macaques. J Neurosci 22:4625–4638
McAlpine D, Jiang D, Shackleton TM, Palmer AR (2000) Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation. J Neurophysiol 83:1356–1365
Mecham JS (1971) Vocalizations of the leopard frog, Rana pipiens, and three related Mexican species. Copeia 3:505–516
Megela AL, Capranica RR (1983) A neural and behavioral study of auditory habituation in the bullfrog, Rana catesbeiana. J Comp Physiol A 151:423–434
Micheyl C, Tian B, Carlyon RP, Rauschecker JP (2005) Perceptual organization of tone sequences in the auditory cortex of awake macaques. Neuron 48:139–148
Moore BC (2008) Basic auditory processes involved in the analysis of speech sounds. Philos Trans R Soc Lond B Biol Sci 363:947–963
Mudry KM, Constantine-Paton M, Capranica RR (1977) Auditory sensitivity of the diencephalon of the leopard frog Rana p. pipiens. J Comp Physiol 114:1–13
Muller JR, Metha AB, Krauskopf J, Lennie P (1999) Rapid adaptation in visual cortex to the structure of images. Science 285:1405–1408
Muller JR, Metha AB, Krauskopf J, Lennie P (2001) Information conveyed by onset transients in responses of striate cortical neurons. J Neurosci 21:6978–6990
Naatanen R (1995) The mismatch negativity: a powerful tool for cognitive neuroscience. Ear Hear 16:6–18
Naatanen R, Alho K (1995) Mismatch negativity—a unique measure of sensory processing in audition. Int J Neurosci 80:317–337
Naatanen R, Tervaniemi M, Sussman E, Paavilainen P, Winkler I (2001) “Primitive intelligence” in the auditory cortex. Trends Neurosci 24:283–288
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
Nelken I, Ulanovsky N (2007) Mismatch negativity and stimulus-specific adaptation in animal models. J Psychophysiol 21:214–223
O’Connor KN, Sutter ML (2000) Global spectral and location effects in auditory perceptual grouping. J Cogn Neurosci 12:342–354
Patterson RD, Nimmo-Smith I, Weber DL, Milroy R (1982) The deterioration of hearing with age: frequency selectivity, the critical ratio, the audiogram, and speech threshold. J Acoust Soc Am 72:1788–1803
Penna M, Lin WY, Feng AS (2001) Temporal selectivity by single neurons in the torus semicircularis of Batrachyla antartandica (Amphibia: Leptodactylidae). J Comp Physiol A 187:901–912
Perez-Gonzalez D, Malmierca MS, Covey E (2005) Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22:2879–2885
Phillips DP, Hall SE, Harrington IA, Taylor TL (1998) “Central” auditory gap detection: a spatial case. J Acoust Soc Am 103:2064–2068
Pinder AC, Palmer AR (1983) Mechanical properties of the frog ear: vibration measurements under free- and closed-field acoustic conditions. Proc R Soc Lond B Biol Sci 219:371–396
Pollak GD, Gittelman JX, Li N, Xie R (2011) 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 273:134–144
Ponnath A, Farris HE (2010) Calcium-dependent control of temporal processing in an auditory interneuron: a computational analysis. J Comp Physiol A 196:613–628
Reches A, Netser S, Gutfreund Y (2010) Interactions between stimulus-specific adaptation and visual auditory integration in the forebrain of the barn owl. J Neurosci 30:6991–6998
Rheinlaender J, Walkowiak W, Gerhardt HC (1981) Directional hearing in the green treefrog: a variable mechanism? Naturwissenschaften 67:430–431
Ringo JL (1996) Stimulus specific adaptation in inferior temporal and medial temporal cortex of the monkey. Behav Brain Res 76:191–197
Ronken DA (1991) Spike discharge properties that are related to the characteristic frequency of single units in the frog auditory nerve. J Acoust Soc Am 90:2428–2440
Roth GL, Aitkin LM, Andersen RA, Merzenich MM (1978) Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 182:661–680
Ryan MJ, Rand AS (2001) Feature weighting in signal recognition and discrimination by the túngara frog. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington DC, pp 86–101
Schul J, Mayo AM, Triblehorn JD (2012) Auditory change detection by a single neuron in an insect. J Comp Physiol A 198(9):695–704
Searcy WA (1992) Song repertoire and mate choice in birds. Am Zool 32:71–80
Spitzer MW, Semple MN (1991) Interaural phase coding in auditory midbrain: influence of dynamic stimulus features. Science 254:721–724
Sun H, Wu SH (2008) Physiological characteristics of postinhibitory rebound depolarization in neurons of the rat’s dorsal cortex of the inferior colliculus studied in vitro. Brain Res 1226:70–81
Swets JA (1986) Indices of discrimination or diagnostic accuracy: their ROCs and implied models. Psychol Bull 99:100–117
Szymanski FD, Garcia-Lazaro JA, Schnupp JW (2009) Current source density profiles of stimulus-specific adaptation in rat auditory cortex. J Neurophysiol 102:1483–1490
Taaseh N, Yaron A, Nelken I (2011) Stimulus-specific adaptation and deviance detection in the rat auditory cortex. PLoS ONE 6:e23369
Tikhonravov D, Neuvonen T, Pertovaara A, Savioja K, Ruusuvirta T, Naatanen R, Carlson S (2010) Dose-related effects of memantine on a mismatch negativity-like response in anesthetized rats. Neuroscience 167:1175–1182
Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6:391–398
Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24:10440–10453
Viemeister NF, Bacon SP (1982) Forward masking by enhanced components in harmonic complexes. J Acoust Soc Am 71:1502–1507
von der BW, Bauerle P, Kossl M, Gaese BH (2009) Correlating stimulus-specific adaptation of cortical neurons and local field potentials in the awake rat. J Neurosci 29:13837–13849
Wilczynski W, Endepols H (2007) Central auditory pathways in anuran amphibians: The anatomical basis of hearing and sound communication. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 221–249
Wilczynski W, Rand AS, Ryan MJ (1995) The processing of spectral cues by the call analysis system of the túngara frog, Physalaemus-pustulosus. Anim Behav 49:911–929
Wilson WW, Walton JP (2002) Background noise improves gap detection in tonically inhibited inferior colliculus neurons. J Neurophysiol 87:240–249
Winer JA, Schreiner CE (2005) The inferior colliculus. Springer, New York
Witte K, Farris HE, Ryan MJ, Wilczynski W (2005) How cricket frog females deal with a noisy world: habitat-related differences in auditory tuning. Behav Ecol 16:571–579
Yang S, Lin W, Feng AS (2009) Wide-ranging frequency preferences of auditory midbrain neurons: roles of membrane time constant and synaptic properties. Eur J Neurosci 30:76–90
Yin TCT, Chan JCK (1988) Neural mechanisms underlying interaural time sensitivity to tones and noise. In: Edelman GM, Gall WE, Cowan WM (eds) Auditory function: neurobiological bases of hearing. Wiley, New York, pp 385–430
Yost WA, Sheft S (1993) Auditory perception. In: Yost WA, Popper AN, Fay RR (eds) Human psychophysics. Springer, New York, pp 193–236
Yu XJ, Xu XX, He S, He J (2009) Change detection by thalamic reticular neurons. Nat Neurosci 12:1165–1170
Zar JH (1999) Biostatistical analysis. Upper Saddle River, New Jersey: Prentice-Hall, Inc
Zhao L, Liu Y, Shen L, Feng L, Hong B (2011) Stimulus-specific adaptation and its dynamics in the inferior colliculus of rat. Neuroscience 181:163–174
Acknowledgments
We thank T. Weyand, C. Canavier, C. Chen, L. Harrison, B. Carlson, T. Forrest, W. Gordon, C. Regan, K. Imaizumi, and two anonymous reviewers for feedback on the project. KLH and HEF were supported in part by a Grass Faculty Fellowship at the Marine Biological Laboratory, Woods Hole, MA (2009). AP and HEF were supported by NIH grant P20RR016816 (to N. Bazan). KH was supported by NSF IOS-0940466.
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Ponnath, A., Hoke, K.L. & Farris, H.E. Stimulus change detection in phasic auditory units in the frog midbrain: frequency and ear specific adaptation. J Comp Physiol A 199, 295–313 (2013). https://doi.org/10.1007/s00359-013-0794-x
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DOI: https://doi.org/10.1007/s00359-013-0794-x