Temporal and spatial coding of periodicity information in the inferior colliculus of awake chinchilla (Chinchilla laniger)
Introduction
Harmonic sounds, commonly found in animal communication sounds and voiced speech, are characterized by a periodic envelope or amplitude modulation (AM). This periodicity is very useful for the recognition of vocalizations and the detection of signals in noise because the peak of the envelope appears repeatedly and predictably above the noise, thereby facilitating signal detection (Zeng et al., 2000, Henry, 1999, Ehrenberger et al., 1999).
The coding of periodicity information in the auditory nerve by activity time-locked to the periodicity of the envelope (Palmer, 1982, Joris and Yin, 1992, Javel, 1980, Delgutte, 1980, Miller and Sachs, 1984, Cariani and Delgutte, 1996, Evans and Palmer, 1980) generates a variety of different periodicity representations in different neuron types of the cochlear nucleus (Frisina et al., 1994, Frisina et al., 1990a, Frisina et al., 1990b, Moller, 1973, Moller, 1974, Rhode, 1995, Rhode and Greenberg, 1994). A neuronal model has been suggested that utilizes these informations for a temporal analysis of signal periodicity which, to a first approximation, corresponds to a correlation and takes place in the brainstem and in the midbrain (Langner, 1981, Langner, 1983, Langner, 1988, Langner, 1992, Langner and Schreiner, 1988, Langner and Schreiner, 1996). The processing mechanisms of the model are similar to the one already suggested by Licklider, 1951, Licklider, 1954, Licklider, 1959, including delayed responses and a coincidence of activity of delayed and undelayed responses as basic processing elements.
In all mammals, the inferior colliculus (IC) is the major midbrain nucleus for integration of auditory information from the brainstem. Units at different central nucleus of inferior colliculus (ICC) locations have been found to be tuned not only to a certain pure tone frequency but also to specific AM frequencies (Langner and Schreiner, 1988). A systematic spatial distribution of modulation frequencies in the ICC, at least of some units, has been suggested (Schreiner and Langner, 1988, Langner, 1992, Langner, 1997, Heil et al., 1995, Langner et al., 1999).
Periodicity information of up to several hundred Hertz is still present to a certain degree in the temporal response patterns of many ICC neurons. However, firing-rate-based periodicity tuning especially for higher modulation frequencies potentially reflects a transformation of temporal into rate/space information of periodicity pitch at this level of the auditory system (Epping and Eggermont, 1986, Langner, 1992). Evidence of periodicity maps has been obtained with electrophysiological recordings in the auditory midbrain of cat (Schreiner and Langner, 1988), in the forebrain of mynah birds (Hose et al., 1987), the auditory cortex of gerbils (Schulze and Langner, 1997), and with optical recording in cat cortex (Langner et al., 1997b). Magnetoencephalography also provided evidence compatible with an orthogonal map of frequency and periodicity information in human auditory cortex (Langner et al., 1997a).
The goal of this study was to re-evaluate several aspects of temporal information coding in the auditory midbrain of an awake animal model. In particular, we investigated
- 1.
whether the rate and synchronization representation of AM signals in the awake animals differs from anesthetized preparations;
- 2.
whether units with tonic and phasic tone responses in the ICC differ in their coding of AM information;
- 3.
whether there are gradients for periodicity information in frequency-band laminae;
- 4.
whether a latency gradient exists for post-synaptic, spiking responses;
- 5.
whether such a gradient exists for mostly pre-synaptic activity as assessed with evoked potentials (EPs);
- 6.
whether there is a co-variation of onset latency and best modulation frequency (BMF).
Section snippets
Surgery
As experimental animals we used adult chinchillas (Chinchilla laniger) of both sexes from the institute’s stock. Preparation of animals was performed under deep halothane anesthesia (0.5–1 vol%; Halocarbon Laboratories, Inc., Hackensack, NJ, USA) and local analgesia (Gingicain; Hoechst AG, Frankfurt, Germany). Body temperature was maintained at 37°C using a feedback-controlled heating blanket. The skin over the skull of the recording (left) side was partly removed. Then the brain over the IC
Neuronal responses to pure tone bursts
From the ICC 901 single and multiple units, that is small clusters of 2–5 units, were recorded in 13 awake chinchillas. In most cases the number of units ranged from one to three, as judged during experiments by highly resolved unit responses on an oscilloscope and as indicated by low average spike rates (see Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6).
All units were tested for their responsiveness to pure tones at 70 dB SPL. BF values were tonotopically organized within ICC with the tonotopic
Advantage and disadvantage of recording in awake animals
It is known from different studies that anesthesia has an influence on activity in the auditory system (Kuwada et al., 1989, Wallhäusser-Franke and Langner, 1999). Although it cannot be excluded that anesthesia influences temporal coding especially of higher modulation frequencies, most investigations of periodicity coding have been performed in anesthetized animals. In awake Guinea fowl high BMFs up to 800 Hz and synchronization to high modulation frequencies up to 1200 Hz were found (Langner,
Conclusions
The questions raised in Section 1 may be answered as follows:
- 1.
The representation of AM signals in the awake animals are very similar to that in anesthetized preparations; however, a consequence of our recordings in awake preparations may be that some units preferred modulation frequencies even above 1 kHz.
- 2.
Units with tonic and phasic tone responses differ in their coding of AM information: good phase coupling to modulation frequencies was obtained mainly in phasic units.
- 3.
A gradient for periodicity
Acknowledgements
We thank Ulrich Bibel and Stefan Bleeck for technical support. We also like to thank C. Schreiner and unknown reviewers for detailed and useful comments. This study was supported by the Deutsche Forschungsgemeinschaft.
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