Early Postnatal Development of Spontaneous and Acoustically Evoked Discharge Activity of Principal Cells of the Medial Nucleus of the Trapezoid Body: AnIn VivoStudy in Mice

Abstract

The calyx of Held synapse in the medial nucleus of the trapezoid body of the auditory brainstem has become an established in vitro model to study the development of fast glutamatergic transmission in the mammalian brain. However, we still lack in vivo data at this synapse on the maturation of spontaneous and sound-evoked discharge activity before and during the early phase of acoustically evoked signal processing (i.e., before and after hearing onset). Here we report in vivo single-unit recordings in mice from postnatal day 8 (P8) to P28 with a specific focus on developmental changes around hearing onset (P12). Data were obtained from two mouse strains commonly used in brain slice recordings: CBA/J and C57BL/6J. Spontaneous discharge rates progressively increased from P8 to P13, initially showing bursting patterns and large coefficients of variation (CVs), which changed to more continuous and random discharge activity accompanied by gradual decrease of CV around hearing onset. From P12 on, sound-evoked activity yielded phasic-tonic discharge patterns with discharge rates increasing up to P28. Response thresholds and shapes of tuning curves were adult-like by P14. A gradual shortening in response latencies was observed up to P18. The three-dimensional tonotopic organization of the medial nucleus of the trapezoid body yielded a high-to-low frequency gradient along the mediolateral and dorsoventral but not in the rostrocaudal axes. These data emphasize that models of signal transmission at the calyx of Held based on in vitro data have to take developmental changes in firing rates and response latencies up to the fourth postnatal week into account.

Spatiotemporal pattern of action potential firing in developing inner hair cells of the mouse cochlea

“…In the mammalian cochlea, it has been proposed that hair cells from the basal coil of the immature cochlea display more sustained activity (8). However, we show that IHCs from the basal coil fire APs in a bursting-like mode, making their activity pattern indistinguishable from that of apical cells, which is consistent with rhythmic activity in the developing auditory pathway (23,(25)(26)(27). The agreement between our measurements performed at room and physiological temperature exclude this parameter as a culprit of interstudy differences.…”

Morphological and Functional Continuum Underlying Heterogeneity in the Spiking Fidelity at the Calyx of Held SynapseIn Vitro

“…To further mimic in vivo conditions in which spontaneous activity is usually present (Hermann et al, 2007), we recorded cell-attached I AP evoked by high-frequency test trains at 35°C after a conditioning train (4 s at 50 Hz). The conditioning frequency of 50 Hz was selected based on values in the in vivo study performed in mice by Lorteije et al (2009), which reported an average spontaneous frequency of ϳ70 Hz, and the studies by Kopp-Scheinpflug et al (2008) and Sonntag et al (2009), which reported an average spontaneous frequency of ϳ30 Hz. After the recordings performed at 35°C, the bath temperature was once again reduced to room temperature, and EPSCs during 100 -300 Hz trains were recorded.…”

Similar Intracellular Ca2+Requirements for Inactivation and Facilitation of Voltage-Gated Ca2+Channels in a Glutamatergic Mammalian Nerve Terminal

“…Auditory brainstem circuits discharge at high rates during sound stimulation and show varying levels of spontaneous AP firing even in the complete absence of sound (Friauf and Ostwald, 1988;Taberner and Liberman, 2005;Tolnai et al, 2008;Sonntag et al, 2009). Within the MNTB of adult rats, spontaneous discharge rates vary between zero and 133 Hz (mean 29 Hz, Tolnai et al, 2008).…”

“…Such elevations of the global volume average [Ca 2ϩ ] i are easily achieved during repetitive AP firing, especially at higher frequencies when individual APevoked [Ca 2ϩ ] i transients start to summate. Since auditory circuits discharge at high rates during sound stimulation and show varying levels of spontaneous AP firing even in the complete absence of sound (Friauf and Ostwald, 1988;Taberner and Liberman, 2005;Tolnai et al, 2008;Sonntag et al, 2009), presynaptic VGCCs at the calyx of Held and presumably also in other auditory terminals predominantly expressing Ca V 2.1 channels will be subject to strong Ca 2ϩ -dependent regulation.…”