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Spectral integration plasticity in cat auditory cortex induced by perceptual training

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Abstract

We investigated the ability of cats to discriminate differences between vowel-like spectra, assessed their discrimination ability over time, and compared spectral receptive fields in primary auditory cortex (AI) of trained and untrained cats. Animals were trained to discriminate changes in the spectral envelope of a broad-band harmonic complex in a 2-alternative forced choice procedure. The standard stimulus was an acoustic grating consisting of a harmonic complex with a sinusoidally modulated spectral envelope (“ripple spectrum”). The spacing of spectral peaks was conserved at 1, 2, or 2.66 peaks/octave. Animals were trained to detect differences in the frequency location of energy peaks, corresponding to changes in the spectral envelope phase. Average discrimination thresholds improved continuously during the course of the testing from phase-shifts of 96° at the beginning to 44° after 4–6 months of training with a 1 ripple/octave spectral envelope. Responses of AI single units and small groups of neurons to pure tones and ripple spectra were modified during perceptual discrimination training with vowel-like ripple stimuli. The transfer function for spectral envelope frequencies narrowed and the tuning for pure tones sharpened significantly in discriminant versus naïve animals. By contrast, control animals that used the ripple spectra only in a lateralization task showed broader ripple transfer functions and narrower pure-tone tuning than naïve animals.

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References

  • Ahissar M, Hochstein S (1993) Attentional control of early perceptual learning. Proc Natl Acad Sci USA 90:5718–5722

    Article  PubMed  CAS  Google Scholar 

  • Allard TA, Clark SA, Jenkins WM, Merzenich MM (1991) Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly. J Neurophysiol 66:1048–1058

    PubMed  CAS  Google Scholar 

  • Amagai A, Dooling RJ, Shamma S, Kidd TL, Lohr B (1999) Detection of modulation in spectral envelopes and linear-rippled noises by budgerigars (Melopsittacus undulatus). J Acoust Soc Am 10:2029–2035

    Article  Google Scholar 

  • Bakin JS, South DA, Weinberger NM (1996) Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance. Behav Neurosci 110:905–913

    Article  PubMed  CAS  Google Scholar 

  • Baru AV (1975) Discrimination of synthesized vowels /a/ and /i/ with varying parameters (fundamental frequency, intensity, duration and number of formants) in dog. In: Fant G, Tatham MAA (eds) Auditory analysis and perception of speech. Academic, London, pp 91–101

    Google Scholar 

  • Beitel RE, Schreiner CE, Merzenich MM (1999) Spectral receptive field plasticity in auditory cortex of owl monkeys trained with sinusoidally amplitude modulated (SAM) tones. Assoc Res Otolaryngol Abstr 21:201

    Google Scholar 

  • Bernstein LR, Green DM (1987) Detection of simple and complex changes of spectral shape. J Acoust Soc Am 82:1587–1592

    Article  PubMed  CAS  Google Scholar 

  • Bilsen FA, ten Kate JH, Buunen TJ, Raatgever J (1975) Responses of single units in the cochlear nucleus of the cat to cosine noise. J Acoust Soc Am 58:858–866

    Article  PubMed  CAS  Google Scholar 

  • Calhoun B, Schreiner CE (1998) Spectral envelope coding in cat primary auditory cortex: linear and non-linear effects of stimulus characteristics. Eur J Neurosci 10:926–940

    Article  PubMed  CAS  Google Scholar 

  • Cheung SW, Nagarajan SS, Bedenbaugh PH, Schreiner CE, Wang X, Wong A (2001) Auditory cortical neuron response differences under isoflurane versus pentobarbital anesthesia. Hear Res 56:115–127

    Article  Google Scholar 

  • Delgutte B, Kiang NYS (1984) Speech coding in the auditory nerve. I. Vowel-like sounds. J Acoust Soc Am 75:866–878

    Article  PubMed  CAS  Google Scholar 

  • DeValois RL, DeValois KK (1990) Spatial vision. Oxford Science Publication, Oxford

    Google Scholar 

  • Dewson JH (1964) Speech sound discrimination by cats. Science 144:555–556

    Article  PubMed  Google Scholar 

  • Edeline J-M (1999) Learning-induced physiological plasticity in the thalamo-cortical sensory system: a critical evaluation of recpetive field plastiicity, map changes and their potential mechanisms. Prog Neurobiol 57:165–224

    Article  PubMed  CAS  Google Scholar 

  • Eggermont JJ (1995) Representation of a voice onset time continuum in primary auditory cortex of the cat. J Acoust Soc Am 98:911–920

    Article  PubMed  CAS  Google Scholar 

  • Ehret G, Schreiner CE (1997) Frequency resolution and spectral integration (critical band analysis) in single units of the cat primary auditory cortex. J Comp Physiol A 181:635–650

    Article  PubMed  CAS  Google Scholar 

  • Escabi M, Schreiner CE (2002) Nonlinear processing of auditory neurons revealed with naturalistic spectro-temporal envelopes. J Neurosci 22:4114–4131

    PubMed  CAS  Google Scholar 

  • Festen JM, Plomp R (1981) Relations between auditory functions in normal hearing. J Acoust Soc Am 70:356–369

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JL (1955) A difference limen for vowel formant frequency. J Acoust Soc Am 27:613–617

    Article  Google Scholar 

  • Gallistel CR (2003) Conditioning from an information processing perspective. Behav Processes 62:89–101

    Article  PubMed  Google Scholar 

  • Green DM, Swets JA (1966) Signal detection theory. Wiley, New York

    Google Scholar 

  • Greenwood DG (1974) Critical bandwidth in man and some other species in relation to the traveling wave envelope. In: Moskowitz HR et al (eds) Sensation and measurement. D Reidel Publishing Co, Dordrecht, pp 231–239

    Google Scholar 

  • Hillier D, Miller J (1991) Auditory-contrast sensitivity in normal and hearing-impaired listeners. J Acoust Soc Am 89:1938

    Article  Google Scholar 

  • Keeling D, Schreiner CE, Jenkins WM (1992) Discrimination of formant shifts in vowel-like ripple spectra. Assoc Res Otolaryngol Abstr 14:201

    Google Scholar 

  • Kilgard MP, Pandya PK, Vazquez J, Gehi A, Schreiner CE, Merzenich MM (2001) Sensory input directs spatial and temporal plasticity in primary auditory cortex. J Neurophysiol 86:326–338

    PubMed  CAS  Google Scholar 

  • Klein DJ, Simon JZ, Shamma SA (2000) Robust spectro-temporal reverse correlation for the auditory system: optimizing stimulus design. J Comput Neurosci 9:85–111

    Article  PubMed  CAS  Google Scholar 

  • Kowalski N, Depireux DA, Shamma SA (1996) Analysis of dynamic spectra in ferret primary auditory cortex. 1. Characteristics of single-unit responses to moving ripple spectra. J Neurophysiol 76:3503–3523

    PubMed  CAS  Google Scholar 

  • Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2002) Hearing after congenital deafness: central auditory plasticity and sensory deprivation. Cereb Cortex 12:797–807

    Article  PubMed  CAS  Google Scholar 

  • Kuhl PK, Miller JD (1975) Speech perception by the chinchilla: voiced-voiceless distinction in alveolar plosive consonants. Science 190:69–72

    Article  PubMed  CAS  Google Scholar 

  • Kuhl PK, Padden DM (1982) Enhanced discriminability at the phonetic boundaries for the voicing feature in macaques. Percept Psychophys 32:542–550

    PubMed  CAS  Google Scholar 

  • Kuhl PK, Padden DM (1983) Enhanced discriminability at the phonetic boundaries for the place feature in macaques. J Acoust Soc Am 73:1003–1010

    Article  PubMed  CAS  Google Scholar 

  • Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115–142

    Article  PubMed  CAS  Google Scholar 

  • Langner G, Schreiner CE (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60:1799–1822

    PubMed  CAS  Google Scholar 

  • Li W, Piech V, Gilbert CD (2004) Perceptual learning and top-down influences in primary visual cortex. Nat Neurosci 7:651–657

    Article  PubMed  CAS  Google Scholar 

  • Linden JF, Liu RC, Sahan M, Schreiner CE, Merzenich MM (2003) Spectrotemporal structure of receptive fields in areas AI and AAF of mouse auditory cortex. J Neurophysiol 90:2660–2675

    Article  PubMed  Google Scholar 

  • Middlebrooks JC, Bierer JA, Snyder RL (2005) Cochlear implants: the view from the brain. Curr Opin Neurobiol 15:488–493

    Article  PubMed  CAS  Google Scholar 

  • Miller LM, Escabi MA, Read HL, Schreiner CE (2002) Spectrotemporal receptive fields in the lemnsical auditory thalamus and cortex. J Neurophysiol 87:516–527

    PubMed  Google Scholar 

  • O’Connor KN, Barruel P, Sutter ML (2000) Global processing of spectrally complex sounds in macaques (Macaca mullata) and humans. J Comp Physiol A 186:903–912

    Article  PubMed  CAS  Google Scholar 

  • Ohl FW, Scheich H (2005) Learning-induced plasticity in animal and human auditory cortex. Curr Opin Neurobiol 15:470–477

    Article  PubMed  CAS  Google Scholar 

  • Polley DB, Heiser MA, Blake DT, Schreiner CE. Merzenich MM (2004) Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. Proc Natl Acad Sci USA 101:16351–16356

    Article  PubMed  CAS  Google Scholar 

  • Polley DB, Steinberg EE, Merzenich MM (2006) Perceptual learning directs auditory cortical map plasticity through top-down influences. J Neurosci 26:4970–4982

    Article  PubMed  CAS  Google Scholar 

  • Pick GF (1980) Level dependence of psychophysical frequency resolution and auditory filter shape. J Acoust Soc Am 68:1085–1095

    Article  PubMed  CAS  Google Scholar 

  • Pickles JO (1975) Normal critical bands in the cat. Acta Otolaryngol 80:245–254

    Article  PubMed  CAS  Google Scholar 

  • Prosen CA, Moody DB, Sommers MS, Stebbins WC (1990) Frequency discrimination in the monkey. J Acoust Soc Am 88:2152–2158

    Article  PubMed  CAS  Google Scholar 

  • Raggio MW, Schreiner CE (1999) Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. III: Activation patterns in long- and short-term deafness. J Neurophysiol 82:3506–3526

    PubMed  CAS  Google Scholar 

  • Read HL, Winer JA, Schreiner CE (2001) Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proc Natl Acad Sci USA 98:8042–8047

    Article  PubMed  CAS  Google Scholar 

  • Recanzone GH, Schreiner CE, Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 1:87–103

    Google Scholar 

  • Recanzone GH, Schreiner CE, Sutter ML, Beitel R, Merzenich MM (1999) Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey. J Comp Neurol 415:460–481

    Article  PubMed  CAS  Google Scholar 

  • Rhode WS, Greenberg S (1994) Encoding of amplitude modulation in the cochlear nucleus of the cat. J Neurophysiol 7:1797–1825

    Google Scholar 

  • Rubinstein JT (2004) How cochlear implants encode speech. Curr Opin Otolaryngol Head Neck Surg 12:444–448

    PubMed  Google Scholar 

  • Sachs MB, Young ED (1979) Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. J Acoust Soc Am 66:470–479

    Article  PubMed  CAS  Google Scholar 

  • Scharf B (1970) Critical bands. In: Tobias JV (eds) Foundations of modern auditory theory. Vol I. Academic, New York, pp 159–202

    Google Scholar 

  • Schreiner CE (1998) Spatial distribution of responses to simple and complex sounds in primary auditory cortex. Audiol Neurootol 3:104–122

    Article  PubMed  CAS  Google Scholar 

  • Schreiner CE, Calhoun BM (1994) Spectral envelope coding in cat primary auditory cortex: properties of ripple transfer functions. Aud Neurosci 1:39–61

    Google Scholar 

  • Schreiner CE, Mendelson JR (1990) Functional topography of cat primary auditory cortex: distribution of integrated excitation. J Neurophysiol 64:1442–1459

    PubMed  CAS  Google Scholar 

  • Schreiner CE, Sutter ML (1992) Topography of excitatory bandwidth in cat primary auditory cortex: single-neuron versus multiple-neuron recordings. J Neurophysiol 68:1487–1502

    PubMed  CAS  Google Scholar 

  • Schreiner CE, Read HL, Sutter ML (2000) Modular organization of frequency integration in primary auditory cortex. Ann Rev Neurosci 23:501–529

    Article  PubMed  CAS  Google Scholar 

  • Shamma SA, Versnel H, Kowalski N (1995) Ripple analysis in the ferret primary auditory cortex. I. Response characteristics of single units to sinusoidally rippled spectra. Aud Neurosci 1:233–254

    Google Scholar 

  • Shipley C, Carterette EC, Buchwald JS (1991) The effects of articulation on the acoustical structure of feline vocalizations. J Acoust Soc Am 89:902–909

    Article  PubMed  CAS  Google Scholar 

  • Sinnott JM (1989) Detection and discrimination of synthetic English vowels by Old World monkeys (Cercophithecus, Macaca) and humans. J Acoust Soc Am 86:557–565

    Article  PubMed  CAS  Google Scholar 

  • Sinnott JM, Kreiter NA (1991) Differential sensitivity to vowel continua in Old World monkeys (Macaca) and humans. J Acoust Soc Am 89:2421–2429

    Article  PubMed  CAS  Google Scholar 

  • Sommers MS, Moody DB, Prosen CA, Stebbins WC (1992) Formant frequency discrimination by Japanese macaques (Macaca fuscata). J Acoust Soc Am 91:3499–3510

    Article  PubMed  CAS  Google Scholar 

  • Steinschneider M, Arezzo JC, Vaughan HG Jr (1990) Tonotopic features of speech-evoked activity in primate auditory cortex. Brain Res 519:158–168

    Article  PubMed  CAS  Google Scholar 

  • Supin AY, Popov VV, Milekhina ON, Tarakanov MB (1994) Frequency resolving power measured by rippled noise. Hear Res 78:31–40

    Article  PubMed  Google Scholar 

  • ten Kate JH, van Bekkum MF (1988) Synchrony-dependent autocorrelation in eighth-nerve-fiber response to rippled noise. J Acoust Soc Am 84:2092–2102

    Article  PubMed  Google Scholar 

  • Thompson M, Porter B, O’Bryan J, Heffner HE, Heffner RS (1990) A syringe-pump food-paste dispenser. Behav Res Methods Instrum Comput 22:49–450

    Google Scholar 

  • Van Veen TM, Houtgast T (1985) Spectral sharpness and vowel dissimilarity. J Acoust Soc Am 77:628–634

    Article  PubMed  Google Scholar 

  • Versnel H, Shamma SA (1998) Spectral-ripple representation of steady-state vowels in primary auditory cortex. J Acoust Soc Am 103:2502–2514

    Article  PubMed  CAS  Google Scholar 

  • Wang K, Shamma SA (1995) Representation of acoustic signals in the primary auditory cortex. IEEE Trans Audio Speech Process 3:382–395

    Article  Google Scholar 

  • Wang X, Sachs MB (1994) Neural encoding of single-formant stimuli in the cat II. Responses of anteroventral cochlear nucleus units. J Neurophysiol 71:59–78

    PubMed  CAS  Google Scholar 

  • Wang X, Merzenich MM, Beitel R, Schreiner CE (1995) Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J Neurophysiol 74:2685–2706

    PubMed  CAS  Google Scholar 

  • Witte RS, Kipke DR (2005) Enhanced contrast sensitivity in auditory cortex as cats learn to discriminate sound frequencies. Brain Res Cogn Brain Res 23:171–184

    Article  PubMed  Google Scholar 

  • Weinberger NM, Diamond DM (1988) Dynamic modulation of the auditory system by associative learning. In: Edelman GM, Gall WE, Cowan WM (eds) Auditory function—neurobiological bases of hearing, Wiley, New York, pp 485–512

    Google Scholar 

  • Wörgötter F, Eysel UT (1987) Quantitative determination of orientational and directional components in the response of visual cortical cells to moving stimuli. Biol Cybern 57:349–355

    Article  PubMed  Google Scholar 

  • Wörgötter F, Grundel O, Eysel UT (1990) Quantification and comparison of cell properties in cat’s striate cortex determined by different types of stimuli. Eur J Neurosci 2:928–941

    Article  PubMed  Google Scholar 

  • Wong S, Schreiner CE (2003) Representation of stop-consonants in cat primary auditory cortex: intensity dependence. Speech Commun 41:93–106

    Article  Google Scholar 

  • Yost WA (1982) The dominance region and ripple noise pitch: a test of the peripheral weighting model. J Acoust Soc Am 72:416–425

    Article  PubMed  CAS  Google Scholar 

  • Young ED, Sachs MB (1979) Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers. J Acoust Soc Am 66:1381–1403

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by NIDCD 02260, NIMH077970, the Max Kade Foundation, the Coleman Memorial Fund, and Hearing Research Inc. We thank Dr. W. M. Jenkins for help with the LabVIEW behavioral testing program, Dr. Craig Atencio for analytical support, and Drs. R. Beitel and J. A. Winer for comments on the manuscript.

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Authors and Affiliations

  1. North Island College, Courtenay, BC, V9N 8N6, Canada

    M. Diane Keeling

  2. Coleman Memorial Laboratory, W.M. Keck Center for Integrative Neuroscience, Department of Otolaryngology, University of California San Francisco, San Francisco, CA, 94143-0732, USA

    Katharina Krüger & Christoph E. Schreiner

  3. Scientific Learning Corporation, 300 Frank H. Ogawa Plaza, Suite 500, Oakland, CA, 94612-2040, USA

    Barbara M. Calhoun

  4. Department of Hearing and Speech Sciences, Vanderbilt Kennedy Center for Human Development, Vanderbilt University, Nashville, TN, 37232-8548, USA

    Daniel B. Polley

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  1. M. Diane Keeling
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  2. Barbara M. Calhoun
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  3. Katharina Krüger
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  4. Daniel B. Polley
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  5. Christoph E. Schreiner
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Correspondence to Christoph E. Schreiner.

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Keeling, M.D., Calhoun, B.M., Krüger, K. et al. Spectral integration plasticity in cat auditory cortex induced by perceptual training. Exp Brain Res 184, 493–509 (2008). https://doi.org/10.1007/s00221-007-1115-9

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