Spinal cords: Symphonies of interneurons across species

Abstract

Vertebrate movement is orchestrated by spinal inter- and motor neurons that, together with sensory and cognitive input, produce dynamic motor behaviors. These behaviors vary from the simple undulatory swimming of fish and larval aquatic species to the highly coordinated running, reaching and grasping of mice, humans and other mammals. This variation raises the fundamental question of how spinal circuits have changed in register with motor behavior. In simple, undulatory fish, exemplified by the lamprey, two broad classes of interneurons shape motor neuron output: ipsilateral-projecting excitatory neurons, and commissural-projecting inhibitory neurons. An additional class of ipsilateral inhibitory neurons is required to generate escape swim behavior in larval zebrafish and tadpoles. In limbed vertebrates, a more complex spinal neuron composition is observed. In this review, we provide evidence that movement elaboration correlates with an increase and specialization of these three basic interneuron types into molecularly, anatomically, and functionally distinct subpopulations. We summarize recent work linking neuron types to movement-pattern generation across fish, amphibians, reptiles, birds and mammals.

Spinal V1 Inhibitory Interneuron Clades Differ in Birthdate, Projections to Motoneurons and Heterogeneity

“…Relationships between V1 clades may extend to phylogeny. Most genetic subclasses of spinal interneurons increase in genetic and functional diversity from zebrafish to mice (Wilson and Sweeney, 2023). V1 interneurons are present in all vertebrate species from fishes with swimming locomotion to mammals with limbed terrestrial locomotion, but they show low diversity in zebrafish (Kimura and Higashijima, 2019) and large heterogeneity in mice (Bikoff et al, 2016).…”

Insights into the mechanisms of neuron generation and specification in the zebrafish ventral spinal cord

“…Numerous studies have presented compelling evidence indicating a remarkable similarity in the key classes of spinal interneurons involved in movement control, gene expression patterns, and transcriptional gene regulatory networks responsible for establishing the spinal neuronal circuitry between zebrafish and mouse (Table 4) [17,24,95,96]. Despite the significant evolutionary distance between vertebrates, this parallelism suggests a shared basis in their spinal neuronal circuitry.…”

Sensory and central contributions to motor pattern generation in a spiking, neuro-mechanical model of the salamander spinal cord

“…The basic repertoire of motor outputs and several anatomical and genetic properties of CPG, brain stem and sensory circuits appear to be largely conserved across vertebrate species [1, 12, 18–22]. However, evolution also gave rise to specialized CPG and sensorimotor circuits that allowed new species to adapt to their habitat and to meet the specific needs of each species.…”

“…Recent advances in molecular genomics and optogenetics - mostly in the mouse and the zebrafish - combined with traditional electrophysiological and anatomical experiments have identified anatomically and functionally distinct reticulospinal and spinal CPG neuronal populations, which are shared across these and other vertebrate species [5, 22, 29]. Reticulospinal neurons (RS) in the brain stem relay motor commands from the mesencephalic locomotor region (MLR) to the spinal interneurons to trigger/terminate a locomotion episode, control the steering, frequency and speed of locomotion and change the expressed locomotor pattern [30–36].…”

“…Similarly, in the salamander, low level stimulation in the MLR evokes slow walking, while high level stimulation evokes swimming at higher movement frequencies [37]. Genetically identified classes of CPG interneurons are responsible for the coordination of different body parts during locomotion [22]. For example, in the zebrafish and tadpoles, chains of commissural glycinergic V0d neurons and ipsilateral glutamatergic CHx10 positive V2a (called dINs in tadpoles) neurons are responsible for the generation of the alternating left-right rhythm and forward wave propagation during swimming.…”