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Passive Synaptic Normalization and Input Synchrony-Dependent Amplification of Cortical Feedback in Thalamocortical Neuron Dendrites
journal contribution
posted on 2023-05-20, 02:07 authored by William ConnellyWilliam Connelly, Crunelli, V, Errington, ACThalamocortical neurons have thousands of synaptic connections from layer VI corticothalamic neurons distributed across their dendritic trees. Although corticothalamic synapses provide significant excitatory input, it remains unknown how different spatial and temporal input patterns are integrated by thalamocortical neurons. Using dendritic recording, 2-photon glutamate uncaging, and computational modeling, we investigated how rat dorsal lateral geniculate nucleus thalamocortical neurons integrate excitatory corticothalamic feedback. We find that unitary corticothalamic inputs produce small somatic EPSPs whose amplitudes are passively normalized and virtually independent of the site of origin within the dendritic tree. Furthermore, uncaging of MNI glutamate reveals that thalamocortical neurons have postsynaptic voltage-dependent mechanisms that can amplify integrated corticothalamic input. These mechanisms, involving NMDA receptors and T-type Ca(2+)channels, require temporally synchronous synaptic activation but not spatially coincident input patterns. In hyperpolarized thalamocortical neurons, T-type Ca(2+)channels produce nonlinear amplification of temporally synchronous inputs, whereas asynchronous inputs are not amplified. At depolarized potentials, the input-output function for synchronous synaptic input is linear but shows enhanced gain due to activity-dependent recruitment of NMDA receptors. Computer simulations reveal that EPSP amplification by T-type Ca(2+)channels and NMDA receptors occurs when synaptic inputs are either clustered onto individual dendrites or when they are distributed throughout the dendritic tree. Consequently, postsynaptic EPSP amplification mechanisms limit the "modulatory" effects of corticothalamic synaptic inputs on thalamocortical neuron membrane potential and allow these synapses to act as synchrony-dependent "drivers" of thalamocortical neuron firing. These complex thalamocortical input-output transformations significantly increase the influence of corticothalamic feedback on sensory information transfer.
History
Publication title
Journal of NeuroscienceVolume
36Issue
13Pagination
3735-3754ISSN
0270-6474Department/School
Tasmanian School of MedicinePublisher
Soc NeurosciencePlace of publication
11 Dupont Circle, Nw, Ste 500, Washington, USA, Dc, 20036Rights statement
Copyright 2016 Connelly et al. Licensed under Creative Commons Attribution 4.0 International (CC BY 4.0) https://creativecommons.org/licenses/by/4.0/Repository Status
- Open