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Brain Topography

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01.05.2015 | Original Paper

A New and Fast Characterization of Multiple Encoding Properties of Auditory Neurons

verfasst von: Boris Gourévitch, Florian Occelli, Quentin Gaucher, Yonane Aushana, Jean-Marc Edeline

Erschienen in: Brain Topography | Ausgabe 3/2015

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Abstract

The functional properties of auditory cortex neurons are most often investigated separately, through spectrotemporal receptive fields (STRFs) for the frequency tuning and the use of frequency sweeps sounds for selectivity to velocity and direction. In fact, auditory neurons are sensitive to a multidimensional space of acoustic parameters where spectral, temporal and spatial dimensions interact. We designed a multi-parameter stimulus, the random double sweep (RDS), composed of two uncorrelated random sweeps, which gives an easy, fast and simultaneous access to frequency tuning as well as frequency modulation sweep direction and velocity selectivity, frequency interactions and temporal properties of neurons. Reverse correlation techniques applied to recordings from the primary auditory cortex of guinea pigs and rats in response to RDS stimulation revealed the variety of temporal dynamics of acoustic patterns evoking an enhanced or suppressed firing rate. Group results on these two species revealed less frequent suppression areas in frequency tuning STRFs, the absence of downward sweep selectivity, and lower phase locking abilities in the auditory cortex of rats compared to guinea pigs.

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Aertsen AM, Johannesma PI (1981) The spectro-temporal receptive field. A functional characteristic of auditory neurons. Biol Cybern 42:133–143CrossRefPubMed

Aertsen AMHJ, Johannesma PIM, Hermes DJ (1980) Spectro-temporal receptive fields of auditory neurons in the grassfrog. II. Analysis of the stimulus-event relation for tonal stimuli. Biol Cybernetics 38:235–248. doi:10.1007/BF00337016 CrossRef

Aertsen AM, Olders JH, Johannesma PI (1981) Spectro-temporal receptive fields of auditory neurons in the grassfrog. III. Analysis of the stimulus-event relation for natural stimuli. Biol Cybern 39:195–209CrossRefPubMed

Ahrens MB, Linden JF, Sahani M (2008) Nonlinearities and contextual influences in auditory cortical responses modeled with multilinear spectrotemporal methods. J Neurosci 28:1929–1942CrossRefPubMed

Atencio CA, Blake DT, Strata F et al (2007) Frequency-modulation encoding in the primary auditory cortex of the awake owl monkey. J Neurophysiol 98:2182–2195CrossRefPubMed

Barbour DL, Wang X (2003) Contrast tuning in auditory cortex. Science 299:1073–1075. doi:10.1126/science.1080425 CrossRefPubMedCentralPubMed

Blake DT, Merzenich MM (2002) Changes of AI receptive fields with sound density. J Neurophysiol 88:3409–3420. doi:10.1152/jn.00233.2002 CrossRefPubMed

Brosch M, Schreiner CE (1997) Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol 77:923–943PubMed

Brosch M, Schreiner CE (2000) Sequence sensitivity of neurons in cat primary auditory cortex. Cereb Cortex 10:1155–1167CrossRefPubMed

Brosch M, Schulz A, Scheich H (1999) Processing of sound sequences in macaque auditory cortex: response enhancement. J Neurophysiol 82:1542–1559PubMed

Carruthers IM, Natan RG, Geffen MN (2013) Encoding of ultrasonic vocalizations in the auditory cortex. J Neurophysiol 109:1912–1927. doi:10.1152/jn.00483.2012 CrossRefPubMedCentralPubMed

Christianson GB, Sahani M, Linden JF (2008) The consequences of response nonlinearities for interpretation of spectrotemporal receptive fields. J Neurosci 28:446–455CrossRefPubMed

David SV, Mesgarani N, Fritz JB, Shamma SA (2009) Rapid synaptic depression explains nonlinear modulation of spectro-temporal tuning in primary auditory cortex by natural stimuli. J Neurosci 29:3374–3386. doi:10.1523/JNEUROSCI.5249-08.2009 CrossRefPubMedCentralPubMed

De Boer R, Kuyper P (1968) Triggered correlation. IEEE Trans Biomed Eng 15:169–179CrossRefPubMed

deCharms RC, Blake DT, Merzenich MM (1998) Optimizing sound features for cortical neurons. Science 280:1439–1443CrossRefPubMed

Depireux DA, Simon JZ, Klein DJ, Shamma SA (2001) Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. J Neurophysiol 85:1220–1234PubMed

DiMattina C, Wang X (2006) Virtual vocalization stimuli for investigating neural representations of species-specific vocalizations. J Neurophysiol 95:1244–1262CrossRefPubMed

Doron NN, Ledoux JE, Semple MN (2002) Redefining the tonotopic core of rat auditory cortex: physiological evidence for a posterior field. J Comp Neurol 453:345–360. doi:10.1002/cne.10412 CrossRefPubMed

Edeline JM (2003) The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Exp Brain Res 153:554–572CrossRefPubMed

Edeline JM, Weinberger NM (1993) Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. Behav Neurosci 107:82–103CrossRefPubMed

Edeline JM, Dutrieux G, Manunta Y, Hennevin E (2001) Diversity of receptive field changes in auditory cortex during natural sleep. Eur J Neurosci 14:1865–1880CrossRefPubMed

Eggermont JJ (1994) Temporal modulation transfer functions for AM and FM stimuli in cat auditory cortex. Effects of carrier type, modulating waveform and intensity. Hear Res 74:51–66CrossRefPubMed

Eggermont JJ (1998) Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. J Neurophysiol 80:2743–2764PubMed

Eggermont JJ (2002) Temporal modulation transfer functions in cat primary auditory cortex: separating stimulus effects from neural mechanisms. J Neurophysiol 87:305–321PubMed

Eggermont JJ, Smith GM (1995) Synchrony between single-unit activity and local field potentials in relation to periodicity coding in primary auditory cortex. J Neurophysiol 73:227–245PubMed

Eggermont JJ, Aertsen AM, Johannesma PI (1983a) Prediction of the responses of auditory neurons in the midbrain of the grass frog based on the spectro-temporal receptive field. Hear Res 10:191–202CrossRefPubMed

Eggermont JJ, Johannesma PM, Aertsen AM (1983b) Reverse-correlation methods in auditory research. Q Rev Biophys 16:341–414CrossRefPubMed

Elhilali M, Fritz JB, Chi TS, Shamma SA (2007) Auditory cortical receptive fields: stable entities with plastic abilities. J Neurosci 27:10372–10382CrossRefPubMed

Epping WJ, Eggermont JJ (1985) Single-unit characteristics in the auditory midbrain of the immobilized grassfrog. Hear Res 18:223–243CrossRefPubMed

Epping WJ, Eggermont JJ (1986a) Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. I. Stimulation with acoustic clicks. Hear Res 24:37–54CrossRefPubMed

Epping WJ, Eggermont JJ (1986b) Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. II. Stimulation with amplitude modulated sound. Hear Res 24:55–72CrossRefPubMed

Escabi MA, Schreiner CE (2002) Nonlinear spectrotemporal sound analysis by neurons in the auditory midbrain. J Neurosci 22:4114–4131PubMed

Fritz J, Shamma S, Elhilali M, Klein D (2003) Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat Neurosci 6:1216–1223. doi:10.1038/nn1141 CrossRefPubMed

Gaese BH, Ostwald J (1995) Temporal coding of amplitude and frequency modulation in the rat auditory cortex. Eur J Neurosci 7:438–450CrossRefPubMed

Games KD, Winer JA (1988) Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hear Res 34:1–25CrossRefPubMed

Gaucher Q, Edeline J-M, Gourévitch B (2012) How different are the local field potentials and spiking activities? Insights from multi-electrodes arrays. J Physiol Paris 106:93–103. doi:10.1016/j.jphysparis.2011.09.006 CrossRefPubMed

Gaucher Q, Huetz C, Gourévitch B, Edeline JM (2013) Cortical inhibition reduces information redundancy at presentation of communication sounds in the primary auditory cortex. J Neurosci 33(26):10713–10728CrossRef

Goldberg JM, Brown PB (1968) Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J Neurophysiol 31:639–656PubMed

Gourévitch B, Edeline J-M (2011) Age-related changes in the guinea pig auditory cortex: relationship with brainstem changes and comparison with tone-induced hearing loss. Eur J Neurosci 34:1953–1965. doi:10.1111/j.1460-9568.2011.07905.x CrossRefPubMed

Gourévitch B, Eggermont JJ (2007) Spatial representation of neural responses to natural and altered conspecific vocalizations in cat auditory cortex. J Neurophysiol 97:144–158CrossRefPubMed

Gourévitch B, Doisy T, Avillac M, Edeline JM (2009a) Follow-up of latency and threshold shifts of auditory brainstem responses after single and interrupted acoustic trauma in guinea pig. Brain Res 1304:66–79CrossRefPubMed

Gourévitch B, Norena A, Shaw G, Eggermont JJ (2009b) Spectrotemporal receptive fields in anesthetized cat primary auditory cortex are context dependent. Cereb Cortex 19:1448–1461CrossRefPubMed

Heffner HE, Heffner RS, Contos C, Ott T (1994) Audiogram of the hooded Norway rat. Hear Res 73:244–247CrossRefPubMed

Heil P, Rajan R, Irvine DR (1992) Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I: effects of variation of stimulus parameters. Hear Res 63:108–134CrossRefPubMed

Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577. doi:10.1152/physrev.00029.2003 CrossRefPubMed

Kaur S, Lazar R, Metherate R (2004) Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J Neurophysiol 91:2551–2567CrossRefPubMed

Kelly JB, Masterton B (1977) Auditory sensitivity of the albino rat. Journal of Comparative and Physiological Psychology 91:930–936. doi:10.1037/h0077356 CrossRefPubMed

Kilgard MP, Merzenich MM (1999) Distributed representation of spectral and temporal information in rat primary auditory cortex. Hear Res 134:16–28CrossRefPubMedCentralPubMed

Klein DJ, Depireux DA, Simon JZ, Shamma SA (2000) Robust spectrotemporal reverse correlation for the auditory system: optimizing stimulus design. J Comput Neurosci 9(1):85–111CrossRefPubMed

Kowalski N, Versnel H, Shamma SA (1995) Comparison of responses in the anterior and primary auditory fields of the ferret cortex. J Neurophysiol 73:1513–1523PubMed

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

Kowalski N, Depireux DA, Shamma SA (1996b) Analysis of dynamic spectra in ferret primary auditory cortex. II. Prediction of unit responses to arbitrary dynamic spectra. J Neurophysiol 76:3524–3534PubMed

Laudanski J, Edeline J-M, Huetz C (2012) Differences between spectro-temporal receptive fields derived from artificial and natural stimuli in the auditory cortex. PLoS ONE 7:e50539. doi:10.1371/journal.pone.0050539 CrossRefPubMedCentralPubMed

Lee YW, Schetzen M (1965) Measurement of the Wiener Kernels of a non-linear system by cross-correlation. Int J Control 2:237–254. doi:10.1080/00207176508905543 CrossRef

Lesica NA, Grothe B (2008) Dynamic spectrotemporal feature selectivity in the auditory midbrain. J Neurosci 28:5412–5421. doi:10.1523/JNEUROSCI.0073-08.2008 CrossRefPubMed

Machens CK, Wehr MS, Zador AM (2004) Linearity of cortical receptive fields measured with natural sounds. The Journal of Neuroscience 24:1089–1100CrossRefPubMed

Manunta Y, Edeline JM (1999) Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow-wave sleep. Eur J Neurosci 11:2134–2150CrossRefPubMed

Mendelson JR, Cynader MS (1985) Sensitivity of cat primary auditory cortex (AI) neurons to the direction and rate of frequency modulation. Brain Res 327:331–335CrossRefPubMed

Mendelson JR, Grasse KL (1992) A comparison of monaural and binaural responses to frequency modulated (FM) sweeps in cat primary auditory cortex. Exp Brain Res 91:435–454CrossRefPubMed

Mendelson JR, Schreiner CE, Sutter ML, Grasse KL (1993) Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps. Exp Brain Res 94:65–87CrossRefPubMed

Miller LM, Escabí MA, Read HL, Schreiner CE (2001) Functional convergence of response properties in the auditory thalamocortical system. Neuron 32:151–160CrossRefPubMed

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

Moller AR (1973) Statistical evaluation of the dynamic properties of cochlear nucleus units using stimuli modulated with pseudorandom noise. Brain Res 57:443–456CrossRefPubMed

Nagarajan SS, Cheung SW, Bedenbaugh P et al (2002) Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. J Neurophysiol 87:1723–1737PubMed

Nelken I, Versnel H (2000) Responses to linear and logarithmic frequency-modulated sweeps in ferret primary auditory cortex. Eur J Neurosci 12:549–562CrossRefPubMed

Nelken I, Prut Y, Vaadia E, Abeles M (1994) In search of the best stimulus: an optimization procedure for finding efficient stimuli in the cat auditory cortex. Hear Res 72:237–253CrossRefPubMed

Orduña I, Mercado E III, Gluck MA, Merzenich MM (2001) Spectrotemporal sensitivities in rat auditory cortical neurons. Hear Res 160:47–57. doi:10.1016/S0378-5955(01)00339-2 CrossRefPubMed

Pienkowski M, Eggermont JJ (2011) Sound frequency representation in primary auditory cortex is level tolerant for moderately loud, complex sounds. J Neurophysiol 106:1016–1027. doi:10.1152/jn.00291.2011 CrossRefPubMed

Pienkowski M, Shaw G, Eggermont JJ (2009) Wiener–Volterra characterization of neurons in primary auditory cortex using poisson-distributed impulse train inputs. J Neurophysiol 101:3031–3041. doi:10.1152/jn.91242.2008 CrossRefPubMedCentralPubMed

Polley DB, Steinberg EE, Merzenich MM (2006) Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci 26:4970–4982. doi:10.1523/JNEUROSCI.3771-05.2006 CrossRefPubMed

Rabinowitz NC, Willmore BDB, Schnupp JWH, King AJ (2012) Spectrotemporal contrast kernels for neurons in primary auditory cortex. J Neurosci 32:11271–11284. doi:10.1523/JNEUROSCI.1715-12.2012 CrossRefPubMedCentralPubMed

Ricketts C, Mendelson JR, Anand B, English R (1998) Responses to time-varying stimuli in rat auditory cortex. Hear Res 123:27–30CrossRefPubMed

Ringach D, Shapley R (2004) Reverse correlation in neurophysiology. Cognitive Science 28:147–166. doi:10.1207/s15516709cog2802_2 CrossRef

Robertson D, Irvine DR (1989) Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J Comp Neurol 282:456–471. doi:10.1002/cne.902820311 CrossRefPubMed

Rutkowski RG, Shackleton TM, Schnupp JW et al (2002) Spectrotemporal receptive field properties of single units in the primary, dorsocaudal and ventrorostral auditory cortex of the guinea pig. Audiol Neurootol 7:214–227CrossRefPubMed

Rutkowski RG, Miasnikov AA, Weinberger NM (2003) Characterisation of multiple physiological fields within the anatomical core of rat auditory cortex. Hear Res 181:116–130CrossRefPubMed

Sally SL, Kelly JB (1988) Organization of auditory cortex in the albino rat: sound frequency. J Neurophysiol 59:1627–1638PubMed

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

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

Schreiner CE, Urbas JV (1988) Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields. Hear Res 32:49–63CrossRefPubMed

Shamma SA, Fleshman JW, Wiser PR, Versnel H (1993) Organization of response areas in ferret primary auditory cortex. J Neurophysiol 69:367–383PubMed

Shechter B, Depireux DA (2007) Stability of spectro-temporal tuning over several seconds in primary auditory cortex of the awake ferret. Neuroscience 148:806–814CrossRefPubMed

Sutter ML, Schreiner CE, McLean M et al (1999) Organization of inhibitory frequency receptive fields in cat primary auditory cortex. J Neurophysiol 82:2358–2371PubMed

Theunissen FE, Sen K, Doupe AJ (2000) Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J Neurosci 20:2315–2331PubMed

Valentine PA, Eggermont JJ (2004) Stimulus dependence of spectro-temporal receptive fields in cat primary auditory cortex. Hear Res 196:119–133. doi:10.1016/j.heares.2004.05.011 CrossRefPubMed

Wallace MN, Palmer AR (2008) Laminar differences in the response properties of cells in the primary auditory cortex. Exp Brain Res 184:179–191. doi:10.1007/s00221-007-1092-z CrossRefPubMed

Wallace MN, Rutkowski RG, Palmer AR (2000) Identification and localisation of auditory areas in guinea pig cortex. Exp Brain Res 132:445–456CrossRefPubMed

Wang X (2000) On cortical coding of vocal communication sounds in primates. Proc Natl Acad Sci USA 97:11843–11849CrossRefPubMedCentralPubMed

Wetzel W, Ohl FW, Wagner T, Scheich H (1998) Right auditory cortex lesion in Mongolian gerbils impairs discrimination of rising and falling frequency-modulated tones. Neurosci Lett 252:115–118CrossRefPubMed

Zhang LI, Tan AY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424:201–205CrossRefPubMed

Zhao L, Zhaoping L (2011) Understanding auditory spectro-temporal receptive fields and their changes with input statistics by efficient coding principles. PLoS Comput Biol 7:e1002123. doi:10.1371/journal.pcbi.1002123 CrossRefPubMedCentralPubMed

Zilles K, Wree A, Dausch N (1990) Anatomy of the neocortex; neurochemical organization. In: Kolb B, Tees RC (eds) The cerebral cortex of the rat. MIT Press, Cambridge, MA, pp 113–150

Titel: A New and Fast Characterization of Multiple Encoding Properties of Auditory Neurons
verfasst von: Boris Gourévitch
Florian Occelli
Quentin Gaucher
Yonane Aushana
Jean-Marc Edeline
Publikationsdatum: 01.05.2015
Verlag: Springer US
Erschienen in: Brain Topography / Ausgabe 3/2015
Print ISSN: 0896-0267
Elektronische ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-014-0375-5

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