Advertisement

Journal of Comparative Physiology A

, Volume 194, Issue 8, pp 693–700 | Cite as

Stimulus-dependent oscillations and evoked potentials in chinchilla auditory cortex

  • Paul H. Delano
  • Elizabeth Pavez
  • Luis Robles
  • Pedro E. Maldonado
Original Paper

Abstract

Besides the intensity and frequency of an auditory stimulus, the length of time that precedes the stimulation is an important factor that determines the magnitude of early evoked neural responses in the auditory cortex. Here we used chinchillas to demonstrate that the length of the silent period before the presentation of an auditory stimulus is a critical factor that modifies late oscillatory responses in the auditory cortex. We used tetrodes to record local-field potential (LFP) signals from the left auditory cortex of ten animals while they were stimulated with clicks, tones or noise bursts delivered at different rates and intensity levels. We found that the incidence of oscillatory activity in the auditory cortex of anesthetized chinchillas is dependent on the period of silence before stimulation and on the intensity of the auditory stimulus. In 62.5% of the recordings sites we found stimulus-related oscillations at around 8–20 Hz. Stimulus-induced oscillations were largest and consistent when stimuli were preceded by 5 s of silence and they were absent when preceded by less than 500 ms of silence. These results demonstrate that the period of silence preceding the stimulus presentation and the stimulus intensity are critical factors for the presence of these oscillations.

Keywords

Auditory cortex Chinchilla Oscillations Local field potential Tetrode 

Abbreviations

EP

Evoked potential

LFP

Local field potential

Notes

Acknowledgments

We thank Bethany Schneider, Fernando Ramirez and Carlos Hamamé for comments on a previous version of the manuscript and Fernando Vergara for technical assistance. This work was supported by FONDECYT 1020970, Iniciativa Científica Milenio ICM P01-007F, PhD Scholarship CONICYT to PHD and PG-42-2004. The experiments reported here comply with the “Principles of Animal Care” (publication No. 86-23, revised 1985 of the NIH) and also with the current Chilean laws (CBA #098 FMUCH).

References

  1. Adrian ED (1950) The electrical activity of the mammalian olfactory bulb. Electroencephalogr Clin Neurophysiol 2:377–388PubMedCrossRefGoogle Scholar
  2. Barth DS, MacDonald KD (1996) Thalamic modulation of high-frequency oscillating potentials in auditory cortex. Nature 383:78–81PubMedCrossRefGoogle Scholar
  3. Brosch M, Budinger E, Scheich H (2002) Stimulus-related gamma oscillations in primate auditory cortex. J Neurophysiol 87:2715–2725PubMedGoogle Scholar
  4. Burkard RF, Secor CA, Salvi RJ (1999) Near-field responses from the round window, inferior colliculus, and auditory cortex of the unanesthetized chinchilla: manipulations of noiseburst level and rate. J Acoust Soc Am 106:304–312PubMedCrossRefGoogle Scholar
  5. Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929PubMedCrossRefGoogle Scholar
  6. Cotillon-Williams N, Edeline JM (2003) Evoked oscillations in the thalamo-cortical auditory system are present in anesthetized but not in unanesthetized rats. J Neurophysiol 89:1968–1984PubMedCrossRefGoogle Scholar
  7. Cotillon-Williams N, Edeline JM (2004) Evoked oscillations in unit recordings from the thalamo-cortical auditory system: an aspect of temporal processing or the reflection of hyperpolarized brain states? Acta Neurobiol Exp (Wars) 64:253–270Google Scholar
  8. Cotillon N, Edeline JM (2000) Tone-evoked oscillations in the rat auditory cortex result from interactions between the thalamus and reticular nucleus. Eur J NeuroSci 12:3637–3650PubMedCrossRefGoogle Scholar
  9. Cotillon N, Nafati M, Edeline JM (2000) Characteristics of reliable tone-evoked oscillations in the rat thalamo-cortical auditory system. Hear Res 142:113–130PubMedCrossRefGoogle Scholar
  10. Dinse HR, Kruger K, Akhavan AC, Spengler F, Schoner G, Schreiner CE (1997) Low-frequency oscillations of visual, auditory, and somatosensory cortical neurons evoked by sensory stimulation. Int J Psychophysiol 26:205–227PubMedCrossRefGoogle Scholar
  11. Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ (1988) Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol Cybern 60:121–130PubMedCrossRefGoogle Scholar
  12. Eggermont JJ (1991) Rate and synchronization measures of periodicity coding in cat primary auditory cortex. Hear Res 56:153–167PubMedCrossRefGoogle Scholar
  13. Eggermont JJ (1992) Stimulus induced and spontaneous rhythmic firing of single units in cat primary auditory cortex. Hear Res 61:1–11PubMedCrossRefGoogle Scholar
  14. 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 73:227–245PubMedGoogle Scholar
  15. Erchova I, Kreck G, Heinemann U, Herz AV (2004) Dynamics of rat entorhinal cortex layer II and III cells: characteristics of membrane potential resonance at rest predict oscillation properties near threshold. J Physiol 560:89–110PubMedCrossRefGoogle Scholar
  16. Franowicz MN, Barth DS (1995) Comparison of evoked potentials and high-frequency (gamma-band) oscillating potentials in rat auditory cortex. J Neurophysiol 74:96–112PubMedGoogle Scholar
  17. Friedman-Hill S, Maldonado PE, Gray CM (2000) Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations. Cereb Cortex 10:1105–1116PubMedCrossRefGoogle Scholar
  18. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends in Cog Neurosci 9:474–480CrossRefGoogle Scholar
  19. Fries P, Nikolić D, Singer W (2007) The gamma cycle. Trends Neurosci 7:309–316CrossRefGoogle Scholar
  20. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563PubMedCrossRefGoogle Scholar
  21. Galambos R, Rose JE, Bromiley RB, Hughes JR (1952) Microelectrode studies on medial geniculate body of cat. II. Response to clicks. J Neurophysiol 15:359–380PubMedGoogle Scholar
  22. Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86:1698–1702PubMedCrossRefGoogle Scholar
  23. Gray CM, Maldonado PE, Wilson M, McNaughton B (1995) Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J Neurosci Methods 63:43–54PubMedCrossRefGoogle Scholar
  24. Gray CM, Viana di Prisco G (1997) Stimulus-dependent neuronal oscillations and local synchronization in striate cortex of the alert cat. J Neurosci 17:3239–3253PubMedGoogle Scholar
  25. Gray CM (1999) The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24:31–47PubMedCrossRefGoogle Scholar
  26. Grenier F, Timofeev I, Steriade M (1998) Leading role of thalamic over cortical neurons during postinhibitory rebound excitation. Proc Natl Acad Sci U S A 95:13929–13934PubMedCrossRefGoogle Scholar
  27. Harel N, Mori N, Sawada S, Mount RJ, Harrison RV (2000) Three distinct auditory areas of cortex (AI, AII, and AAF) defined by optical imaging of intrinsic signals. Neuroimage 11:302–312PubMedCrossRefGoogle Scholar
  28. Harrison RV, Kakigi A, Hirakawa H, Harel N, Mount RJ (1996) Tonotopic mapping in auditory cortex of the chinchilla. Hear Res 100:157–163PubMedCrossRefGoogle Scholar
  29. Horikawa J, Tanahashi A, Suga N (1994) After-discharges in the auditory cortex of the mustached bat: no oscillatory discharges for binding auditory information. Hear Res 76:45–52PubMedCrossRefGoogle Scholar
  30. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577PubMedCrossRefGoogle Scholar
  31. Kenmochi M, Eggermont JJ (1997) Autonomous cortical rhythms affect temporal modulation transfer functions. NeuroReport 8:1589–1593PubMedCrossRefGoogle Scholar
  32. Kilgard MP, Merzenich MM (1998) Plasticity of temporal information processing in the primary auditory cortex. Nat Neurosci 1:727–731PubMedCrossRefGoogle Scholar
  33. Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115–142PubMedCrossRefGoogle Scholar
  34. Lu T, Liang L, Wang X (2001) Temporal and rate representations of time-varying signals in the auditory cortex of awake primates. Nat Neurosci 4:1131–1138PubMedCrossRefGoogle Scholar
  35. Maldonado PE, Gerstein GL (1996) Reorganization in the auditory cortex of the rat induced by intracortical microstimulation: a multiple single-unit study. Exp Brain Res 112:420–430PubMedGoogle Scholar
  36. Phillips DP, Hall SE, Hollett JL (1989) Repetition rate and signal level effects on neuronal responses to brief tone pulses in cat auditory cortex. J Acoust Soc Am 85:2537–2549PubMedCrossRefGoogle Scholar
  37. Spotorno AE, Zuleta CA, Valladares JP, Deane AL, Jiménez JE (2004) Chinchilla laniger. Mammalian Species 758:1–9CrossRefGoogle Scholar
  38. Tomita M, Eggermont JJ (2005) Cross-correlation and joint spectro-temporal receptive field properties in auditory cortex. J Neurophysiol 93:378–392PubMedCrossRefGoogle Scholar
  39. Whittington MA, Doheny HC, Traub RD, LeBeau FE, Buhl EH (2001) Differential expression of synaptic and nonsynaptic mechanisms underlying stimulus-induced gamma oscillations in vitro. J Neurosci 21:1727–1738PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Paul H. Delano
    • 1
    • 3
    • 4
  • Elizabeth Pavez
    • 1
    • 2
  • Luis Robles
    • 1
  • Pedro E. Maldonado
    • 1
    • 3
  1. 1.Programa de Fisiología y Biofísica, ICBM, Facultad de MedicinaUniversidad de ChileSantiago 7Chile
  2. 2.Escuela de Tecnología Médica, Facultad de MedicinaUniversidad de ChileSantiagoChile
  3. 3.Centro de Neurociencias Integradas, ICMSantiagoChile
  4. 4.Servicio Otorrinolaringología, Hospital Clínico de la Universidad de ChileSantiagoChile

Personalised recommendations