Mechanosensory Stimulation Evokes Acute Concussion-like Behaviour by Activating GIRKs Coupled to Muscarinic Receptors in a Simple Vertebrate

Abstract

Most vertebrates show concussion responses when their heads are hit suddenly by heavy objects. Previous studies have focused on the direct physical injuries to the neural tissue caused by the concussive blow. We study a similar behaviour in a simple vertebrate, the Xenopus Laevis tadpole. We find that concussion-like behaviour can be reliably induced by the mechanosensory stimulation of the head skin without direct physical impacts on the brain. Head skin stimulation activates a cholinergic pathway which then opens G-protein coupled inward-rectifying potassium channels (GIRKs) via postsynaptic M₂ muscarinic receptors to inhibit brainstem neurons critical for the initiation and maintenance of swimming for up to minutes and can explain many features commonly observed immediately after concussion. We propose that some acute symptoms of concussion in vertebrates can be explained by the opening of GIRKs following mechanosensory stimulation to the head.

Significance Statement Most vertebrates have concussion responses when their heads are hit suddenly by heavy objects, rendering the animals momentarily motionless and often unconscious. We study a similar behavior in a simple vertebrate, Xenopus Laevis tadpoles, and find that concussion-like behavior in these tadpoles can be induced reliably by mechanosensory stimulation of the head skin. The head skin stimulation then activates some cholinergic neurons in the brainstem to inhibit the tadpole motor circuit. These results provide a potential explanation why concussion in vertebrates often recovers spontaneously without sustaining clear physical injury to the brain and some acute symptoms of concussion can be a neurophysiological response to specific sensory stimulation.