Synaptic modification in neurons of the central nucleus of the inferior colliculus

Wu, Shu Hui; Lei, Chun; Sivaramakrishnan, Shobhana; Oliver, Douglas L.

doi:10.1016/s0378-5955(02)00375-1

Cited by 36 publications

(51 citation statements)

References 36 publications

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“…In some IC neurons, synaptic depression appears to occur in control conditions, whereas in others, it occurs only when GABA A receptors are blocked. This finding is consistent with the conditions necessary to generate synaptic plasticity in the IC in vitro (Wu et al, 2002), as well as in other systems such as the hippocampus and cerebellum where synaptic depression and potentiation of glutamatergic transmission may be observed normally in some conditions and, in others, more readily when GABA A receptors are blocked (Zucker and Regehr, 2002).…”

Section: Discussionsupporting

confidence: 87%

“…Changes in the shape of the synaptic current with increasing shock strength are likely to reflect differential activation of the glutamate receptors present on IC neurons (Wu et al, 2002) during recruitment. Without the concurrent activation of GABA A synapses, these excitatory inputs cause large and prolonged depolarizations, during which firing block occurs.…”

Section: Discussionmentioning

confidence: 99%

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GABA_ASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

Sivaramakrishnan

Sterbing²,

Filipovic³

et al. 2004

J. Neurosci.

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Neurons in the inferior colliculus (IC) change their firing rates with sound pressure level. Some neurons maintain monotonic increases in firing rate over a wide range of sound intensities, whereas other neurons are monotonic over limited intensity ranges. We examined the conditions necessary for monotonicity in this nucleus in vitro in rat brain slices and in vivo in the unanesthetized rabbit. Our in vitro recordings indicate that concurrent activation of GABA A synapses with excitatory inputs facilitates monotonic increases in firing rate with increases in stimulus strength. In the absence of synaptic inhibition, excitatory input to IC neurons causes large depolarizations that result in firing block and nonmonotonicity. In vivo, although GABA A synapses decrease the firing rate in all IC neurons, they can have opposing effects on rate-level functions. GABAergic inputs activated by all sound intensities maintain monotonicity by keeping the postsynaptic potential below the level at which depolarization block occurs. When these inputs are blocked, firing block can occur and rate-level functions become nonmonotonic. High-threshold GABAergic inputs, in contrast, cause nonmonotonic responses by decreasing the firing rate at high intensities. Our results suggest that a dynamic regulation of the postsynaptic membrane potential by synaptic inhibition is necessary to allow neurons to respond monotonically to a wide range of sound intensities.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

GABA_ASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

Sivaramakrishnan

Sterbing²,

Filipovic³

et al. 2004

J. Neurosci.

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“…Experiments in brain slices offer a controlled environment for the activation of synaptic inputs to ICC neurons and have allowed the pharmacological isolation and identification of specific synaptic currents (Moore et al 1998;Ma et al 2002a, b;Wu et al 2002Wu et al , 2004.…”

Section: Introductionmentioning

confidence: 99%

“…Most brain slice experiments in the rat ICC have been performed on transverse slices (Smith 1992;Li et al 1994Li et al , 1998Li et al , 1999Bal et al 2002;Kraushaar and Backus 2002;Ma et al 2002a, b;Wu et al 2002;N'Gouemo and Morad 2003;Wu et al 2004), cut roughly perpendicular to the ICC layers. Because that plane cuts the laminae, it is likely to sever the dendrites of the flat cells and will cut many inputs to the ICC, particularly those entering from the lateral lemniscus.…”

Section: Introductionmentioning

confidence: 99%

“…This has not been a problem for previous studies focused on the dorsal cortex of IC, because commissural inputs were not cut (Smith 1992;Li et al 1994Li et al , 1998Li et al , 1999. When using the transverse plane, the stimulating electrodes must be placed inside the ventrolateral part of ICC (Wu et al 2002(Wu et al , 2004 or just outside it (Wagner, 1996;Moore et al 1998). This makes it likely that local IC axons are directly stimulated in addition to axons from the lateral lemniscus.…”

Section: Introductionmentioning

confidence: 99%

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Neuronal Responses to Lemniscal Stimulation in Laminar Brain Slices of the Inferior Colliculus

Sivaramakrishnan

Oliver

2005

JARO

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The central nucleus of the inferior colliculus (ICC) receives inputs from all parts of the auditory brainstem and transmits the information to the forebrain. Fibrodendritic laminae of the ICC provide a structural basis for a tonotopic organization, and the interaction of inputs within a single layer is important for ICC processing. Transverse slice planes of the ICC sever the layers and many of the ascending axons that enter through the lateral lemniscus. Consequently, the activity initiated within a lamina by a pure lemniscal stimulus is not well characterized. Here, we use a slice plane that maintains the integrity of the laminae in ICC and allows the axons in the lateral lemniscus to be stimulated at a distance from the ICC. We examined both the postsynaptic currents and potentials of the same neurons to lemniscal stimuli in this laminar brain slice. Our main finding is that lemniscal stimulation evokes prolonged synaptic potentials in ICC neurons. Synaptic potential amplitudes and durations increase with lemniscal shock strength. In õ50% of ICC neurons, the postsynaptic potential is equal in duration to the postsynaptic current, whereas in the remaining neurons it is three to four times longer. Synaptic responses to single shocks or shock trains exhibit plateau potentials that enable sustained firing in ICC neurons. Plateau potentials are evoked by N-methyl-D-aspartate (NMDA) receptor activation, and their amplitudes and durations are regulated by both NMDA-R and gamma-aminobutyric acid A (GABA A )-R activation. These data suggest that in the intact laminae of the ICC, lemniscal inputs initiate sustained firing through monosynaptic and polysynaptic NMDA-mediated synapses regulated by GABA A synapses.

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Biophysical Properties of Inferior Colliculus Neurons

Wu¹

2005

The Inferior Colliculus

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Synaptic modification in neurons of the central nucleus of the inferior colliculus

Cited by 36 publications

References 36 publications

GABA_ASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

GABA_ASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

Neuronal Responses to Lemniscal Stimulation in Laminar Brain Slices of the Inferior Colliculus

Biophysical Properties of Inferior Colliculus Neurons

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Synaptic modification in neurons of the central nucleus of the inferior colliculus

Cited by 36 publications

References 36 publications

GABAASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

GABAASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

Neuronal Responses to Lemniscal Stimulation in Laminar Brain Slices of the Inferior Colliculus

Biophysical Properties of Inferior Colliculus Neurons

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Product

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GABA_ASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

GABA_ASynapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus