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.
Similar content being viewed by others
Abbreviations
- EP:
-
Evoked potential
- LFP:
-
Local field potential
References
Adrian ED (1950) The electrical activity of the mammalian olfactory bulb. Electroencephalogr Clin Neurophysiol 2:377–388
Barth DS, MacDonald KD (1996) Thalamic modulation of high-frequency oscillating potentials in auditory cortex. Nature 383:78–81
Brosch M, Budinger E, Scheich H (2002) Stimulus-related gamma oscillations in primate auditory cortex. J Neurophysiol 87:2715–2725
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 106:304–312
Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929
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 89:1968–1984
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) 64:253–270
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 12:3637–3650
Cotillon N, Nafati M, Edeline JM (2000) Characteristics of reliable tone-evoked oscillations in the rat thalamo-cortical auditory system. Hear Res 142:113–130
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 26:205–227
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 60:121–130
Eggermont JJ (1991) Rate and synchronization measures of periodicity coding in cat primary auditory cortex. Hear Res 56:153–167
Eggermont JJ (1992) Stimulus induced and spontaneous rhythmic firing of single units in cat primary auditory cortex. Hear Res 61:1–11
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 73:227–245
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 560:89–110
Franowicz MN, Barth DS (1995) Comparison of evoked potentials and high-frequency (gamma-band) oscillating potentials in rat auditory cortex. J Neurophysiol 74:96–112
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 10:1105–1116
Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends in Cog Neurosci 9:474–480
Fries P, Nikolić D, Singer W (2007) The gamma cycle. Trends Neurosci 7:309–316
Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563
Galambos R, Rose JE, Bromiley RB, Hughes JR (1952) Microelectrode studies on medial geniculate body of cat. II. Response to clicks. J Neurophysiol 15:359–380
Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86:1698–1702
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 63:43–54
Gray CM, Viana di Prisco G (1997) Stimulus-dependent neuronal oscillations and local synchronization in striate cortex of the alert cat. J Neurosci 17:3239–3253
Gray CM (1999) The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24:31–47
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 95:13929–13934
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 11:302–312
Harrison RV, Kakigi A, Hirakawa H, Harel N, Mount RJ (1996) Tonotopic mapping in auditory cortex of the chinchilla. Hear Res 100:157–163
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 76:45–52
Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577
Kenmochi M, Eggermont JJ (1997) Autonomous cortical rhythms affect temporal modulation transfer functions. NeuroReport 8:1589–1593
Kilgard MP, Merzenich MM (1998) Plasticity of temporal information processing in the primary auditory cortex. Nat Neurosci 1:727–731
Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115–142
Lu T, Liang L, Wang X (2001) Temporal and rate representations of time-varying signals in the auditory cortex of awake primates. Nat Neurosci 4:1131–1138
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 112:420–430
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 85:2537–2549
Spotorno AE, Zuleta CA, Valladares JP, Deane AL, Jiménez JE (2004) Chinchilla laniger. Mammalian Species 758:1–9
Tomita M, Eggermont JJ (2005) Cross-correlation and joint spectro-temporal receptive field properties in auditory cortex. J Neurophysiol 93:378–392
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 21:1727–1738
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).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Delano, P.H., Pavez, E., Robles, L. et al. Stimulus-dependent oscillations and evoked potentials in chinchilla auditory cortex. J Comp Physiol A 194, 693–700 (2008). https://doi.org/10.1007/s00359-008-0340-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-008-0340-4