A specialized spinal circuit for command amplification and directionality during escape behavior

In vertebrates, action selection often involves higher cognition entailing an evaluative process. However, urgent tasks, such as defensive escape, require an immediate implementation of the directionality of escape trajectory, necessitating local circuits. Here we reveal a specialized spinal circuit for the execution of escape direction in adult zebrafish. A central component of this circuit is a unique class of segmentally repeating cholinergic V2a interneurons expressing the transcription factor Chx10. These interneurons amplify brainstem-initiated escape commands and rapidly deliver the excitation via a feedforward circuit to all fast motor neurons and commissural interneurons to direct the escape maneuver. The information transfer within this circuit relies on fast and reliable axo-axonic synaptic connections, bypassing soma and dendrites. Unilateral ablation of cholinergic V2a interneurons eliminated escape command propagation. Thus, in vertebrates, local spinal circuits can implement directionality of urgent motor actions vital for survival.

Motor primitives are determined in early development and are then robustly conserved into adulthood

Motor patterns in legged vertebrates show modularity in both young and adult animals, comprising motor synergies or primitives. Are such spinal modules observed in young mammals conserved into adulthood or altered? Conceivably, early circuit modules alter radically through experience and descending pathways’ activity. We analyze lumbar motor patterns of intact adult rats and the same rats after spinal transection and compare these with adult rats spinal transected 5 days postnatally, before most motor experience, using only rats that never developed hind limb weight bearing. We use independent component analysis (ICA) to extract synergies from electromyography (EMG). ICA information-based methods identify both weakly active and strongly active synergies. We compare all spatial synergies and their activation/drive strengths as proxies of spinal modules and their underlying circuits. Remarkably, we find that spatial primitives/synergies of adult injured and neonatal injured rats differed insignificantly, despite different developmental histories. However, intact rats possess some synergies that differ significantly, although modestly, in spatial structure. Rats injured as adults were more similar in modularity to rats that had neonatal spinal transection than to themselves before injury. We surmise that spinal circuit modules for spatial synergy patterns may be determined early, before postnatal day 5 (P5), and remain largely unaltered by subsequent development or weight-bearing experience. An alternative explanation but equally important is that, after complete spinal transection, both neonatal and mature adult spinal cords rapidly converge to common synergy sets. This fundamental or convergent synergy circuitry, fully determined by P5, is revealed after spinal cord transection.