The ability to move depends on networks of neurons in the spinal cord. Recent research in zebrafish larvae has identified topographic patterns of functional organisation within these networks and shed light on the general principles underlying their development.
Previous research by Mclean et al. has revealed topographic patterns of functional organisation in the spinal cord of the larval zebrafish that underlies its ability to swim at different speeds. In particular, slow movements recruit neurons close to the ventral edge of the spinal cord while more dorsal networks become active as speed increases. Now, Mclean and Fetcho have demonstrated a relationship between the temporal order of differentiation of neurons in the map and the development of motor behaviour.
The fact that the most dorsal neurons are the earliest born suggests a developmental process generating these topographical maps. McLean and Fetcho examined this idea in three stages. First, they filmed Zebrafish larvae to examine developmental changes in swimming movements. This showed that the first movements to develop in 2-day old embryos involve large amplitude lateral head and tail movements characteristic of fast swimming. The smaller movements of the tail characteristic of slow swimming only emerge later in the 4-day old larvae. While larvae make the large movements at high frequencies and the small movements at low frequencies, the embryos made the large movements at all frequencies.
In a second stage, the authors used whole-cell patch recordings to see if there are corresponding differences in patterns of motor neuron firing between embryonic and larval swimming. They induced episodes of fictive swimming in paralysed zebrafish using a brief electrical shock and took recordings from peripheral motor nerves. Comparing embryos and larvae demonstrated that embryonic motor patterns has a short burst duration closely resembling that of high-frequency larval swimming. However, low-frequency movements generated different motor patterns in embryos compared to the larva. These findings mirror the behavioural results and show that the motor neuron circuits generating large-amplitude, fast swimming movements in the larvae are present and functional at the embryonic stage.
Finally, McLean and Fetcho examined the role of excitatory interneurons using transgenic fish expressing the photoconvertible protein Kaede to track neuronal differentiation in vivo. Tracking the emergence of spinal circuits directly in this way showed that one class of excitatory premotor interneurons (circumferential descending cells or CiDs), which are active during escape and fast swimming movements, emerge very early at dorsal locations with younger neurons appearing more ventrally. Another class of excitatory premotor interneuron (multipolar commissural descending cells or MCoDs), however, which are active only at very slow swimming speeds, differentiate very late and are located most ventrally.
These results demonstrate that spinal circuits responsible for fast escape and swimming movements in zebrafish larvae develop first in dorsal locations. Those neurons generating slower movements are layered on below during development, resulting in topographic patterns of recruitment seen in larvae. McLean and Fetcho suggest that this pattern of development may generalise to other tetrapods, including humans where the earliest movements in utero are large-scale startle responses.
