Shaw-like potassium currents in the auditory rhombencephalon throughout embryogenesis

Abstract

The Shaw subfamily of potassium channel genes, including Kv3.1, are highly expressed within the auditory nuclei of the brainstem, where they have been implicated in the characteristic response properties of particular types of neurons. Potassium currents carried by Kv3.1 are voltage-dependent, have a high activation threshold, are slow to inactivate, and are very sensitive to 4-aminopyridine (4-AP) and tetraethylammonium (TEA). We have investigated the developmental appearance of potassium currents in cell cultures from nucleus magnocellularis and its precursor neuroblasts from the acoustico-vestibular anlage of the chicken. Whole-cell patch recordings revealed that high-threshold, sustained, outward currents were present in 91% of neuroblasts. These currents displayed high sensitivities to TEA and 4-AP. The remaining 9% of neuroblasts exhibited only transient outward currents. Most cells (74%) had both a sustained and an initial transient component of outward current. These current types were observed throughout embryogenesis, beginning with the earliest ages (embryonic day [E]2). During proliferation and migration, and early neuronal differentiation, current levels were low; they incremented gradually during the time when the first synapses occur on dendrites and increased 2- to 3-fold just before hatching, when axosomatic synapses form. These findings suggest that the Shaw subfamily of channels in nucleus magnocellularis may be involved in early neuronal development, as well as in synaptic function later on.

Development of synapses and expression of a voltage-gated potassium channel in chick embryonic auditory nuclei

“…The difference between results obtained with these two antibodies was that KvN stained more neurons compared to its counterpart. In addition to these immunohistochemical studies, our lab has also shown that Kv3.1 conductance could be recorded as early as E5 in dissociated neurons by using a patch-clamp technique (Hendriks et al, 1999a). This is earlier than reported by Parameshwaran-Lyer et al (2003), although the antibodies used are presumably the same.…”

“…In the late embryonic stage of E17, KvC appeared as intensely stained perisomatic rings associated with the cell surface, as compared to the patches visible within the perikaryon at E12. This observation suggests a translocation of Kv3.1b channel protein from the cytoplasmic domain onto the cell surface, during the period when there is a large increase in Kv3.1 currents (Hendriks et al, 1999a). This translocation appears to coincide with the formation of the endbulbs of Held of the cochlear nerve axons on the bushy cell bodies, at the time when there is a reorganization of the afferent synapses from the axodendritic to the axosomatic form (Fig.…”

“…These studies have shown that in the absence of synaptic input there is expression of Kv3.1 channel protein. There is also evidence of an up regulation of the conductance associated with Kv3.1 at the developmental stage when synapses form with the cochlear nerve (Hendriks et al, 1999a). In addition, findings by other authors suggest that depolarization can selectively increase the expression of Kv3.1 in auditory neurons (Liu and Kaczmarek, 1998b).…”

“…The early expression of Kv3.1 channel protein has been traced in the bushy cells of NM and principal cells of NL from E5 to E19, in the stages before and after the establishment of synaptic connections (Zhou et al, 2001). A normocytic culture system (Book et al, 1991) has been devised to study Kv3.1 expression in the absence of cochlear input (Feng and Morest, 2001) and with the patch-clamp technique in cells from the same tissue, as early as E2 (Hendriks et al, 1999a). These studies have shown that in the absence of synaptic input there is expression of Kv3.1 channel protein.…”

Neuronal differentiation of the early embryonic auditory hindbrain of the chicken in primary culture

“…Synaptogenesis in the auditory brainstem starts at around E10 (Alladi et al, 2002;Person et al, 2004) and auditory evoked potentials have been recorded as early as E11-E13 (Jackson et al, 1982;Pettigrew et al, 1988). The voltage-gated potassium channel Kv3.1b, which allows fast repolarization of APs, is strongly expressed in the auditory brainstem from early embryonal stages onward (Hendriks et al, 1999b;Parameshwaran et al, 2001, Parameshwaran-Iyer et al, 2003.…”