Spontaneous Multimodal Neural Transmission Suggests That Adult Spinal Networks Maintain an Intrinsic State of Readiness to Execute Sensorimotor Behaviors

Spontaneous action potential discharge (spAP) is both ubiquitous and functionally relevant during neural development. spAP remains a prominent feature of supraspinal networks in maturity, even during unconsciousness. Evidence suggests that spAP persists in mature spinal networks during wakefulness, and one function of spAP in this context could be maintenance of a ‘ready state’ to execute behaviors. The extent to which spAP persists in mature spinal networks during unconsciousness remains unclear, and its function(s), if any, are likewise unresolved. Here, we attempt to reconcile some of the questions and contradictions that emerge from the disintegrated picture of adult spinal spAP currently available. We recorded simultaneously from large populations of spinal interneurons in vivo in male rats, characterizing the spatial distribution of spAP in the lumbar enlargement and identifying subgroups of spontaneously active neurons. We find (1) concurrent spAP throughout the dorso-ventral extent of the gray matter, with a diverse yet strikingly consistent mixture of neuron types across laminae; (2) the proportion of neurons exhibiting spAP in deeper, sensorimotor integrative regions is comparable to that in more superficial, sensory-dominant regions; (3) firing rate, but not spike train variability, varies systematically with region; and (4) spAP includes multimodal neural transmission consistent with executing a spinally-mediated behavior. These findings suggest that adult spAP may continue to support a state of readiness to execute sensorimotor behaviors even during unconsciousness. Such functionality has implications for our understanding of how perception is translated into action, of experience-dependent modification of behavior, and (mal)adaptative responses to injury or disease. IMPACT STATEMENT Neurons often discharge action potentials seemingly spontaneously, that is, in the absence of ongoing behaviors or overt stimuli. This phenomenon is particularly evident during neural development, where spontaneous action potential discharge is ubiquitous in the central nervous system and is crucial to establishing connectivity amongst functionally related groups of neurons. The function(s) of spontaneous action potential discharge in adult spinal networks, if any, have remained enigmatic – especially during unconsciousness. Here, we report evidence that one such function could be to support an intrinsic state of readiness to execute sensorimotor behaviors. This finding has implications for our understanding of how perception is translated into action, of experience-dependent modification of behavior, and (mal)adaptative responses to injury or disease.