Research PaperCholinergic responses of acoustically-characterized cochlear nucleus neurons: An in vivo iontophoretic study in Guinea pig
Introduction
The mammalian cochlear nuclear complex receives descending cholinergic innervation from several sources. Superior olivary complex inputs comprise the collateral projection of medial olivocochlear (MOC) efferent neurons (Benson and Brown, 1990; Brown and Benson, 1992; Brown et al., 1988, 1991), and a separate direct projection from the ventral nuclei of the trapezoid body (Sherriff and Henderson, 1994). Tegmental areas also are known to supply cholinergic input to both the dorsal (DCN) and ventral cochlear nucleus (VCN) (Mellott et al., 2011). The importance of these descending systems in the modulation of ascending auditory information is still a matter of conjecture and the specific neuronal targets that receive cholinergic input within the diverse populations of cell types in the cochlear nuclear complex, is not firmly established. Anatomical studies show that MOC collaterals make excitatory synaptic contacts with dendrites of multipolar neurons in VCN (Benson and Brown, 1990; Benson et al., 1996). Two major populations of multipolar cells in VCN are the d-stellate, thought to correspond to Onset Chopper (Oc) neurons and the T-stellate, thought to correspond to the transient chopper (Ct) and sustained chopper (Cs) neurons (Oertel and Fujino, 2001; Oertel et al., 1990; Smith and Rhode, 1989; Smith et al., 2005). In vivo electrophysiological studies using both intra and extracellular recordings, indicate that onset type and Oc neurons are excited by activation of olivocochlear collaterals (Mulders et al., 2002, 2003, 2007, 2009).
However, in mouse brain slices, excitatory responses to application of cholinergic agonists have only been reported in T-stellate cells and bushy cells (Fujino and Oertel, 2001; Oertel and Fujino, 2001). The latter authors specifically report a lack of cholinergic responses in d-stellate neurons, which evidence suggests correspond to Oc neurons (Oertel et al., 1990; Smith and Rhode, 1989). The present study attempts to resolve some of these conflicts by combining in vivo recording of cholinergic responses of cochlear nucleus (CN) neurons with detailed classification of their acoustic response types.
Section snippets
Animals
Eighteen pigmented guinea pigs were used in this study. All anaesthetic and surgical methods conformed to the Code of Practice of the National Health and Medical Research Council of Australia and were approved by the Animal Ethics Committee of the University of Western Australia. All procedures, anaesthetic and surgical methods have been reported in detail previously (Vogler et al., 2011, 2014). Briefly, animals received a subcutaneous injection of 0.1 ml atropine followed by an intraperitoneal
Results
Table 1 summarizes the results of iontophoretic application of glutamate, glycine, carbachol and acetylcholine. The responses to iontophoretic applications which satisfied the criteria described above (see Methods), were recorded in 82 neurons. Of these, glutamate and glycine responses were tested in 19 and 2 neurons respectively. In the remaining 61 neurons, carbachol responses were tested in 17 and ACh responses in 44 neurons.
With respect to cholinergic responses, no inhibitory effects were
Discussion
The present study has a number of limitations. The strict criteria we chose to apply before accepting drug-related responses as genuine, and the need to fully characterize acoustic response properties of each neuron, means that the final sample size is rather small. In addition, single cell iontophoresis combined with extracellular recording of spike activity suffers from problems of interpretation. For example, a lack of response in terms of spike rate changes does not exclude the possibility
Acknowledgements
Supported by grants from the NHMRC (APP1042623), MHRIF and The University of Western Australia.
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