Abstract
For a biological neural network to be functional, its neurons need to be connected with synapses of appropriate strength, and each neuron needs to appropriately respond to its synaptic inputs. This second aspect of network tuning is maintained by intrinsic plasticity; yet it is often considered secondary to changes in connectivity and mostly limited to adjustments of overall excitability of each neuron. Here we argue that even nonoscillatory neurons can be tuned to inputs of different temporal dynamics and that they can routinely adjust this tuning to match the statistics of their synaptic activation. Using the dynamic clamp technique, we show that, in the tectum of Xenopus tadpole, neurons become selective for faster inputs when animals are exposed to fast visual stimuli but remain responsive to longer inputs in animals exposed to slower, looming, or multisensory stimulation. We also report a homeostatic cotuning between synaptic and intrinsic temporal properties of individual tectal cells. These results expand our understanding of intrinsic plasticity in the brain and suggest that there may exist an additional dimension of network tuning that has been so far overlooked.NEW & NOTEWORTHY We use dynamic clamp to show that individual neurons in the tectum of Xenopus tadpoles are selectively tuned to either shorter (more synchronous) or longer (less synchronous) synaptic inputs. We also demonstrate that this intrinsic temporal tuning is strongly shaped by sensory experiences. This new phenomenon, which is likely to be mediated by changes in sodium channel inactivation, is bound to have important consequences for signal processing and the development of local recurrent connections.
Highlights
It is often assumed, in fields as diverse as connectomics and machine learning, that the main difference between functional and dysfunctional neural networks lies in their connectivity (Bassett and Sporns 2017; Hildebrand et al 2017; Reimann et al 2017; Takemura 2015)
We investigate whether exposure to sensory stimuli with different temporal dynamics would change the intrinsic temporal tuning of sensory neurons in the optic tectum of Xenopus tadpoles
We show that the intrinsic plasticity of tectal neurons supports temporal selectivity, which is shaped by sensory experience and is coordinated with the typical duration of synaptic inputs received by each cell
Summary
In fields as diverse as connectomics and machine learning, that the main difference between functional and dysfunctional neural networks lies in their connectivity (Bassett and Sporns 2017; Hildebrand et al 2017; Reimann et al 2017; Takemura 2015). We know that neurons adjust their spikiness to match the levels of synaptic activation they experience (Aizenman et al 2003; Titley et al 2017), but we know that intrinsic properties can affect more subtle neuronal tuning to different temporal patterns of activation (Azouz and Gray 2000; Branco et al 2010; Fontaine et al 2014; Jarvis et al 2018; Ohtsuki and Hansel 2018; Zbili et al 2019). This raises the question: do neurons use this type of tuning in practice, dynamically adjusting it to the temporal dynamics of their inputs?
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