Electrophysiological Activity of Multifunctional and Behaviorally Specialized Spinal Neurons Involved in Swimming, Scratching, and Flexion Reflex in Turtles

Abstract

The adult turtle spinal cord can generate multiple kinds of limb movements, including swimming, three forms of scratching, and limb withdrawal (flexion reflex), even without brain input and sensory feedback. There are many multifunctional spinal neurons, activated during multiple motor patterns, and some behaviorally specialized neurons, activated during only one. How do multifunctional and behaviorally specialized neurons each contribute to motor output? We analyzed in vivo intracellular recordings of multifunctional and specialized neurons. Neurons tended to spike in the same phase of the hip-flexor activity cycle during swimming and scratching, though one preferred opposite phases. During both swimming and scratching, a larger fraction of multifunctional neurons than specialized neurons were highly rhythmic. One group of multifunctional neurons was active during the hip flexor-on phase and another during the hip flexor-off phase. Thus, hip flexor-extensor alternation may be generated by a subset of multifunctional spinal neurons during both swimming and scratching. Scratch-specialized neurons and flexion reflex-selective neurons may instead trigger their respective motor patterns, by biasing activity of multifunctional neurons. In phase-averaged membrane potentials of multifunctional neurons, trough phases were more highly correlated between swimming and scratching than peak phases, suggesting that rhythmic inhibition plays a greater role than rhythmic excitation. We also provide the first intracellular recording of a turtle swim-specialized neuron: tonically excited during swimming, but inactive during scratching and flexion reflex. It displayed an excitatory postsynaptic potential following each swim-evoking electrical stimulus and thus may be an intermediary between reticulospinal axons and the swimming CPG they activate.Significance StatementWe analyzed in vivo intracellular recordings of multifunctional and behaviorally specialized turtle spinal neurons, including scratch-specialized and flexion reflex-selective neurons. During both swimming and scratching motor patterns, there were more highly rhythmic multifunctional neurons than behaviorally specialized neurons; their rhythmic modulation appeared to be caused mostly by inhibition. Multifunctional neurons may form core elements of central pattern generators, while behaviorally specialized neurons trigger each motor pattern. We also recorded intracellularly the first turtle swim-specialized neuron.