Activity-dependent regulation of synaptic strength and neuronal excitability in central auditory pathways - PubMed (original) (raw)

Review

Activity-dependent regulation of synaptic strength and neuronal excitability in central auditory pathways

Bruce Walmsley et al. J Physiol. 2006.

Abstract

Neural activity plays an important role in regulating synaptic strength and neuronal membrane properties. Attempts to establish guiding rules for activity-dependent neuronal changes have led to such concepts as homeostasis of cellular activity and Hebbian reinforcement of synaptic strength. However, it is clear that there are diverse effects resulting from activity changes, and that these changes depend on the experimental preparation, and the developmental stage of the neural circuits under study. In addition, most experimental evidence on activity-dependent regulation comes from reduced preparations such as neuronal cultures. This review highlights recent results from studies of the intact mammalian auditory system, where changes in activity have been shown to produce alterations in synaptic and membrane properties at the level of individual neurons, and changes in network properties, including the formation of tonotopic maps.

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Figures

Figure 1

Figure 1. Major pathways in the mammalian auditory brainstem

This schematic shows the auditory nerve (AN) arising from the cochlea and making monosynaptic connections with neurons in the cochlea nucleus of the brainstem (AVCN – anteroventral cochlear nucleus). Also shown are some of the major brainstem auditory nuclei: the medial nucleus of the trapezoid body (MNTB), the medial superior olive (MSO) and the lateral superior olive (LSO). Auditory nerve fibres make large excitatory synaptic contacts, the endbulbs of Held, with bushy cells in the AVCN. Globular bushy cells in the AVCN, in turn, make large calyceal contacts, the calyces of Held, with principal cells in the contralateral MNTB. Spherical bushy cells make ipsilateral contacts with the dendrites of neurons in the MSO. Excitatory neurons and synapses are shown in black; inhibitory neurons and synapses are shown in red.

Figure 2

Figure 2. Excitatory synaptic transmission is greater in deaf mice

A, reconstructions from electron micrographs of 4 different endbulbs of Held contacting a bushy cell in the AVCN. B shows the individual synaptic specializations contained within the boutons shown in A. C shows that both AMPA and NMDA components of the synaptic current arising from individual auditory nerve fibres are larger in deaf (dn/dn) mice. D illustrates that delayed asynchronous spontaneous release is much larger in deaf mice (insets). (A adapted from Nicol & Walmsley, 2002, with permission from Blackwell Publishing Ltd, B–D adapted from Oleskevich & Walmsley, 2002, with permission from Blackwell Publishing Ltd.)

Figure 3

Figure 3. MNTB neurons are more excitable in MNTB neurons

A illustrates that MNTB neurons usually respond to depolarizing currents with a single or a few, action potentials, whereas MNTB neurons in deaf (dn/dn) mice respond with multiple action potentials. Panels on the left indicate the up- (arrows up), down- (arrows down) or no change (X) in the magnitude of voltage-activated currents in MNTB neurons from deaf cf. normal mice. Background immunolabelling shows HCN1 immunoreactivity (red) on LSO neurons (green).

Figure 4

Figure 4. Tonotopic gradients of channel expression are disrupted in deaf mice

A illustrates an obvious medial (M) to lateral (L) gradient in pre- and post-synaptic immunolabelling of Kv3.4 channels (red) in MNTB neurons from a normal mouse. B illustrates a summary schematic (adapted from Leao et al. 2005_a_, with permission from Blackwell Publishing Ltd) of the MNTB (green shading) in normal and deaf (dn/dn) mice. Left panel shows the tonotopic (HF, high frequency; LF, low frequency) gradient of high-threshold potassium currents (Kv3.1), low-threshold potassium currents (Kv1.1) and hyperpolarization-activated currents (HCN4). Right panel shows that these gradients are not present in deaf (dn/dn) mice.

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