Burst generation by T-type calcium channels in motor but not sensory thalamus

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. The sensory system needs to effectively reflect information of the world outside otherwise the motor system generates output to decide whether a certain behavior will be done. To gain different purpose, the neurons in two system would apply different principles to process input (“qualitative difference”) by using the cellular and molecular machinery in physiological structure of a single neuron (“quantitative difference”). Examples in previous studies have showed that the sensory neurons cancel input so that carry only novel information in their output while the motor neurons amplify signals in output by adding internally stored information as well as by integrating input from outside. We have proposed that a specific machinery, the voltage-gated ion channels in neurons, of motor but not sensory systems make a strong contribution to spike generation (output), so that only motor neurons display bursts of spikes with an all-or-none character under natural conditions of wakefulness. We tested this hypothesis in the thalamus which consists of the single type of neurons across the regions but is divided into dozens of nuclei to project axons to different sensory or motor cortex. Using a single type of neuron, the difference beyond what is caused by the sensory-motor dimension could be removed. We have recorded neurons in brain slices from 8 sensory and motor regions of rat thalamus, and examined responses to brief depolarizations resembling excitatory postsynaptic potentials (EPSPs). Consistent with this hypothesis, we previously reported that T-type calcium channels (TtCC) do not cause bursts of spikes in visual thalamus but instead serve a homeostatic role in maintaining the causal link between retinogeniculate excitation and spike output. As predicted by theory, TtCC caused larger depolarizations and more spikes in motor (ventrolateral) 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. Other membrane properties also correlated with location of nuclei along the sensory-motor dimension, with lower input resistance and stronger depolarization mediated by H-type cation channels in nuclei closer to motor output. These findings support our hypothesis of a specific difference between sensory and motor neurons at the cellular level. The classification of neurons by the sensory-motor dimension is rational beyond the intact nervous system. It implies two systems would need to achieve different goals, which could provide the insight on how the basic principle that the single neurons use to work is combined in the systemic view.