Tonotopic Gradients of Membrane and Synaptic Properties for Neurons of the Chicken Nucleus Magnocellularis

Abstract

Nucleus magnocellularis (NM) is a division of the avian cochlear nucleus that extracts the timing of auditory signals. We compared the membrane excitability and synaptic transmission along the tonotopic axis of NM. Neurons expressed a Kv1.1 potassium channel mRNA and protein predominantly in the high characteristic frequency (CF) region of NM. In contrast, the expression of Kv1.2 mRNA did not change tonotopically. Neurons also showed tonotopic gradients in resting potential, spike threshold, amplitude, and membrane rectification. All neurons were sensitive to 100 nM dendrotoxin, but the effects were most significant in the high CF neurons. The EPSC recorded by minimal stimulation of auditory nerve fibers (ANFs) was 13 times larger in high CF neurons than in low CF neurons. Moreover, EPSCs were generated in an all-or-none manner in the high CF neurons when stimulus intensity was increased, whereas EPSCs were graded in the low CF neurons, indicating multiple axonal inputs. ANF synaptic terminals were visualized by DiI. ANF formed enfolding end-bulbs of Held around the cell body in the high and middle CF region but not in the low CF region. These observations indicate coordinated gradients of neuronal properties both presynaptically and postsynaptically along the tonotopic axis. Such specializations may be suitable for extracting and preserving the timing information of auditory signals over a wide range of acoustic frequencies.

Tonotopic Specialization of Auditory Coincidence Detection in Nucleus Laminaris of the Chick

“…The immunoreactivity of Kv1.1 in NL was weak and positive especially in the neuropil region even by the present fixation procedure (APC-009; Alomone Labs) (Fukui and Ohmori, 2004). This is in contrast to the observation by Lu et al (2004); Kv1.1 labeling in NL was predominant in the neuronal soma rather than in the neuropil, and the difference may be attributable to the different polyclonal antibody raised against Kv1.1.…”

“…4). Action potentials of Ͻ20 mV in amplitude were also reported in neurons specialized for processing auditory temporal signals, such as octopus cells of mammalian ventral cochlear nucleus (Golding et al, 1999) and chicken NM neurons (Reyes et al, 1994;Fukui and Ohmori, 2004). In these neurons, the DTX-sensitive I LTK is robust.…”

“…In NM of the chicken, the monotonic gradient of the expression of both mRNA and protein of Kv1.1, as well as the DTX-sensitive current were found, increasing toward the high-CF region (Fukui and Ohmori, 2004). In the lateral superior olive of the rat (Barnes-Davies et al, 2004), neurons in the low-CF region expressed higher levels of Kv1 channels than those in the high-CF region, which allows the low-CF neurons to integrate precisely timed binaural signals.…”

“…4Ca and 6 I). The expression of Kv1.1 mRNA and protein was weak in NL compared with NM (Fukui and Ohmori, 2004;Lu et al, 2004). Therefore, it is conceivable that Kv1.2-containing channels mediate the I LTK and contribute to the specialization of middle-CF NL neuron as a coincidence detector.…”

“…4Ca) suggests that Kv1 channels are responsible for I LTK (Grismmer et al, 1994). In situ hybridization studies have shown that NL neurons expressed Kv1.1 and Kv1.2 subunits; in particular, Kv1.2 was predominant in NL (Fukui and Ohmori, 2004). However, the immunopositivity of Kv1.1 in NL was only in the neuropil region (ventral and dorsal sides of cell bodies) and Kv1.2 was negative [sc-11188 (Santa Cruz Biotechnology, Santa Cruz, CA), APC-010 (Alomone Labs)] (Fukui and Ohmori, 2004).…”