Synaptic activity-induced Ca2+ signaling in avian cochlear nucleus magnocellularis neurons

Abstract

Neurons of the avian cochlear nucleus magnocellularis (NM) receive glutamatergic inputs from the spiral ganglion cells via the auditory nerve and feedback GABAergic inputs primarily from the superior olivary nucleus. We investigated regulation of Ca2+ signaling in NM neurons with ratiometric Ca2+ imaging in chicken brain slices. Application of exogenous glutamate or GABA increased the intracellular Ca2+ concentration ([Ca2+]i) in NM neurons. Interestingly, GABA-induced Ca2+ responses persisted into neuronal maturation, in both standard and energy substrate enriched artificial cerebrospinal fluid. More importantly, we found that electrical stimulation applied to the glutamatergic and GABAergic afferent fibers innervating the NM was able to elicit transient [Ca2+]i increases in NM neurons, and the amplitude of the Ca2+ responses increased with increasing frequency and duration of the electrical stimulation. Antagonists for ionotropic glutamate receptors significantly blocked these [Ca2+]i increases, whereas blocking GABAA receptors did not affect the Ca2+ responses, suggesting that synaptically released glutamate but not GABA induced the Ca2+ signaling in vitro. Furthermore, activation of GABAA receptors with exogenous agonists inhibited synaptic activity-induced [Ca2+]i increases in NM neurons, suggesting a role of GABAA receptors in the regulation of Ca2+ homeostasis in the avian cochlear nucleus neurons.

Metabotropic glutamate receptors in auditory processing

“…Readers are referred to a comprehensive review covering these studies (Rubel and Fritzsch, 2002). Recently, we extended these studies by characterizing synaptic activity-induced Ca 2+ signaling and confirming mGluR-induced increase of intracellular Ca 2+ concentration in NM neurons (Wang et al, 2012). …”

Distinct Neural Properties in the Low-Frequency Region of the Chicken Cochlear Nucleus Magnocellularis

“…For optimally performing auditory tasks across sound frequencies, auditory neurons develop gradients of structural, synaptic, and intrinsic properties along the tonotopic axis. In the auditory brainstem, frequency-specific neuronal processing is tuned by tonotopic gradients of ion channel expression ( von Hehn et al, 2004 ; Leao et al, 2006 ; Gazula et al, 2010 ), synaptic transmission and depression ( Köppl, 1994 ; Fukui and Ohmori, 2004 ; Slee et al, 2010 ; Oline and Burger, 2014 ), and inhibitory kinetics ( Tang et al, 2011 ; Wang et al, 2012 ).…”

Distribution of Vesicular Glutamate Transporter 2 and Ionotropic Glutamate Receptors in the Auditory Ganglion and Cochlear Nuclei of Pigeons (Columba livia)

“…The present study demonstrated expression of vGluT2 mRNA in AG neurons. Neurons in the magnocellular and angular nuclei evoke excitatory postsynaptic potentials mediated by AMPA and/or NMDA receptors by stimulation of the auditory nerve (Martin, ; Zhang and Trussell, ,b; MacLeod and Carr, ; Wang et al., ). Raman and Trussell () showed pharmacological evidence of kainate receptors in the magnocellular nucleus.…”

“…They synapse on the auditory ganglion (AG) cells which in turn project to the magnocellular nucleus and angular nucleus in the brainstem (Boord and Rasmussen, ; Takasaka and Smith, ; Parks and Rubel, ). Stimulation of the chick auditory nerve evokes excitatory postsynaptic potentials in neurons of the magnocellular nucleus and angular nucleus mediated by α ‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazole propionic acid (AMPA) and N‐methyl‐D‐aspartate (NMDA) receptors (Zhang and Trussell, ,b; Lawrence et al., ; MacLeod and Carr, ; Wang et al., ). Neurons in the magnocellular and angular nuclei express mRNAs or proteins of three types of glutamate receptors: AMPA, kainate and NMDA receptors (Levin et al., ; Reng et al., ; Parks, ; Karim et al., ).…”