Metabotropic Glutamatergic Signaling Adaptively Controls Trans-thalamic Communication

Abstract

Trans-thalamic circuits link cortical regions through higher-order sensory (HOs) thalamic nuclei to support cognition. These circuits are rich with metabotropic glutamate receptors (mGluRs), whose seconds-long dynamics conflict with the thalamus’s traditional relay role, leaving their function unknown. Here, we present a model of group I mGluR-mediated suppression of K+ leak currents in single neurons. Including mGluRs in a trans-thalamic network of spiking neurons revealed distinct modulatory roles for thalamocortical and corticothalamic mGluRs. In pyramidal neurons, thalamocortical mGluRs strengthen somato-dendritic coupling and dendritic plateau potentials, boosting feedforward propagation of sensory information to enhance decision-making in a detection task. In HOs thalamic neurons, corticothalamic mGluRs temporally integrate inputs to shift thalamic firing from burst to tonic, a prediction supported by pulvinar recordings in behaving animals. This effect increases detection of a novel stimulus (“wake-up call”) while attenuating detection of repeated stimuli. Therefore, mGluRs enable the HOs thalamus to dynamically modulate cortical communication.