Posthearing Developmental Refinement of Temporal Processing in Principal Neurons of the Medial Superior Olive

Abstract

In mammals, principal neurons of the medial superior olive (MSO) exhibit biophysical specializations that enable them to detect soundlocalization cues with microsecond precision. In the present study, we used whole-cell patch recordings to examine the development of the intrinsic electrical properties of these neurons in brainstem slices from postnatal day 14 (P14) to P38 gerbils. In the week after hearing onset (P14 -P21), we observed dramatic reductions in somatic EPSP duration, input resistance, and membrane time constant. Surprisingly, somatically recorded action potentials also dramatically declined in amplitude over a similar period (38 Ϯ 3 to 17 Ϯ 2 mV; ϭ 5.2 d). Simultaneous somatic and dendritic patch recordings revealed that these action potentials were initiated in the axon, which primarily emerged from the soma. In older gerbils, the rapid speed of membrane voltage changes and the attenuation of action potential amplitudes were mediated extensively by low voltage-activated potassium channels containing the Kv1.1 subunit. In addition, whole-cell voltage-clamp recordings revealed that these potassium channels increase nearly fourfold from P14 to P23 and are thus a major component of developmental changes in excitability. Finally, the electrophysiological features of principal neurons of the medial nucleus of the trapezoid body did not change after P14, indicating that posthearing regulation of intrinsic membrane properties is not a general feature of all time-coding auditory neurons. We suggest that the striking electrical segregation of the axon from the soma and dendrites of MSO principal neurons minimizes spike-induced distortion of synaptic potentials and thus preserves the accuracy of binaural comparisons.

Computation of Interaural Time Difference in the Owl's Coincidence Detector Neurons

“…A low input resistance contributes to the short membrane time constant, which is thought to be necessary for ITD computation (Gerstner et al, 1996). Similar low input resistance has also been reported in other auditory coincidence detectors such as the NL neurons of posthatch chicks (Kuba et al, 2005(Kuba et al, , 2006 and the mammalian MSO (Scott et al, 2005).…”

“…This phenomenon has been observed in in vitro studies of NL cells in posthatch chicks (Kuba et al, 2006), neurons of the medial superior olivary nucleus (MSO) of the gerbil (Scott et al, 2005), and octopus cells of the anteroventral cochlear nucleus (Golding et al, 1999), but was not previously confirmed in vivo.…”

“…Remote spike initiation may allow for a lower spike threshold at the spike initiation site, by filtering DC potentials that could inactivate Na channels (Kuba et al, 2006). This configuration could also amplify high-frequency signals at the spike initiation site (Ashida et al, 2007), decreasing backpropagation (Golding et al, 1999;Scott et al, 2005Scott et al, , 2007, and reducing the metabolic cost of high-frequency firing (Ashida et al, 2007).…”

Lateralization of Interimplant Timing and Level Differences in Children Who Use Bilateral Cochlear Implants

“…It has been suggested the normally-developing SOC retains the ability to calibrate ITD sensitivity to changes in head size throughout childhood but that the basic functional structure for processing interaural cues is intact very early in development (Ashmead et al 1991;Scott et al 2005). This raises the question of whether bilateral cochlear implantation provides sufficient information for the proper calibration of the SOC in congenitally deaf children.…”

Medial Superior Olivary Neurons Receive Surprisingly Few Excitatory and Inhibitory Inputs with Balanced Strength and Short-Term Dynamics

“…Neurons in the MSO have a low input resistance (Magnusson et al, 2005;Scott et al, 2005;Chirila et al, 2007), suggesting that large synaptic currents are required for action potential (AP) generation and for inhibitory inputs to have a significant impact. This assumption is supported by ultrastructural evidence for multiple active zones on both excitatory and inhibitory synaptic boutons contacting the MSO (Clark, 1969;Lindsey, 1975;Kiss and Majorossy, 1983;Brunso-Bechtold et al, 1990;Kapfer et al, 2002).…”