Abstract
Although neurons within intact nervous systems can be classified as ‘sensory’ or ‘motor,’ it is not known whether there is any general distinction between sensory and motor neurons at the cellular or molecular levels. Here, we extend and test a theory according to which activation of certain subtypes of voltage-gated ion channel (VGC) generate patterns of spikes in neurons of motor systems, whereas VGC are proposed to counteract patterns in sensory neurons. We previously reported experimental evidence for the theory from visual thalamus, where we found that T-type calcium channels (TtCCs) did not cause bursts of spikes but instead served the function of ‘predictive homeostasis’ to maximize the causal and informational link between retinogeniculate excitation and spike output. Here, we have recorded neurons in brain slices from eight sensory and motor regions of rat thalamus while mimicking key features of natural excitatory and inhibitory post-synaptic potentials. As predicted by theory, TtCC did cause bursts of spikes in motor thalamus. TtCC-mediated responses in motor thalamus were activated at more hyperpolarized potentials and caused larger depolarizations with more spikes than in visual and auditory thalamus. Somatosensory thalamus is known to be more closely connected to motor regions relative to auditory and visual thalamus, and likewise the strength of its TtCC responses was intermediate between these regions and motor thalamus. We also observed lower input resistance, as well as limited evidence of stronger hyperpolarization-induced (‘H-type’) depolarization, in nuclei closer to motor output. These findings support our theory of a specific difference between sensory and motor neurons at the cellular level.
Highlights
The distinction between ‘sensory’ and ‘motor’ is fundamental to popular conceptions of the nervous system
We report results from secondary visual thalamus (LP), primary and secondary somatosensory thalamus (VB and PoM, respectively), primary and secondary auditory thalamus (MGv and MGd, respectively), and a “cognitive” or “pre-motor” nucleus (MD)
It was not our intention to characterize the H-type depolarization, we found that it was twice as large in ventral lateral (VL) as lateral geniculate nucleus (LGN) (Figure 2C) and differed significantly across the five nuclei recorded in dynamic clamp square-wave” (DCSW) and aEPSG protocols
Summary
The distinction between ‘sensory’ and ‘motor’ is fundamental to popular conceptions of the nervous system. Excitatory post-synaptic potentials (EPSPs) conveying current sensory evidence should ideally be the sole proximate cause of spikes in sensory neurons (Sherman and Guillery, 1998; Kay and Phillips, 2011; Fiorillo et al, 2014) We previously tested this by examining the function of T-type calcium channel (TtCC) in thalamocortical (TC) neurons of the lateral geniculate nucleus (LGN) while mimicking natural conditions. We found that TtCC amplified EPSPs toward spike threshold so that EPSPs may or may not cause spikes, depending on their amplitude (Hong et al, 2014) This supports our theory, according to which TtCC in sensory neurons should help to maximize the causal link between synaptic excitation and spikes without themselves causing spikes, through a process we have termed “predictive homeostasis” (Fiorillo et al, 2014; Hong et al, 2014). We have used dynamic clamp to mimic natural synaptic conductances
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