Abstract
The output of individual neurons is dependent on both synaptic and intrinsic membrane properties. While it is clear that the response of an individual neuron can be facilitated or inhibited based on the summation of its constituent synaptic inputs, it is not clear whether subthreshold activity, (e.g. synaptic “noise”- fluctuations that do not change the mean membrane potential) also serve a function in the control of neuronal output. Here we studied this by making whole-cell patch-clamp recordings from 29 mouse thalamocortical relay (TC) neurons. For each neuron we measured neuronal gain in response to either injection of current noise, or activation of the metabotropic glutamate receptor-mediated cortical feedback network (synaptic noise). As expected, injection of current noise via the recording pipette induces shifts in neuronal gain that are dependent on the amplitude of current noise, such that larger shifts in gain are observed in response to larger amplitude noise injections. Importantly we show that shifts in neuronal gain are also dependent on the intrinsic sensitivity of the neuron tested, such that the gain of intrinsically sensitive neurons is attenuated divisively in response to current noise, while the gain of insensitive neurons is facilitated multiplicatively by injection of current noise- effectively normalizing the output of the dLGN as a whole. In contrast, when the cortical feedback network was activated, only multiplicative gain changes were observed. These network activation-dependent changes were associated with reductions in the slow afterhyperpolarization (sAHP), and were mediated at least in part, by T-type calcium channels. Together, this suggests that TC neurons have the machinery necessary to compute multiple output solutions to a given set of stimuli depending on the current level of network stimulation.
Highlights
Individual thalamocortical relay (TC) neurons can mediate nonlinear signal transformations, which may be important for both the gating and information processing functions of the thalamus
We investigated the mechanisms by which TC neurons adjust their sensitivity to simulated network activity and physiologically relevant activity
Our experiments demonstrate that TC neurons display a range of sensitivities, which are significantly modified by the injection of current noise
Summary
Individual thalamocortical relay (TC) neurons can mediate nonlinear signal transformations, which may be important for both the gating and information processing functions of the thalamus. The sign of retinal (feedforward) inputs onto TC neurons determines which mode of firing is recruited to signal specific features of a visual scene [13,14,15,16]. These studies show that individual TC neurons have the cellular machinery necessary to provide adaptive computations over their inputs. Anatomical studies demonstrate that TC neurons receive a wide range of inputs from cortical, subcortical, and peripheral sensory structures [18,19,20] Many of these have addressed the peculiar advantages of the ‘burst’ firing mode [21,22], but during normal processing it is the tonic-firing mode that predominates, providing over 90% of spikes. Simulated network activity reduced gain in a minority of neurons, suggesting that the prevailing level of network activation may perform a normalisation operation, tending to set the sensitivity of neurons at an optimal value
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