In comparison to the clownish stumbling of most of us landlubbers, fish are elegant beasts. They appear to cruise through the water by simply wiggling their bodies back-and-forth in a single (axial) plane. Walking on solid ground looks and feels far more complicated, requiring independent control of multiple limbs along several axes.
Given the evident ease of the fish's locomotor lifestyle, it has been assumed that the spinal networks that control their movements are relatively simple. In particular, it was thought that fish could independently control muscles on the left and right sides of their bodies, but dorsal and ventral muscles within a body quadrant always contracted together. However, a recent study of zebrafish motor circuits has gutted this assumption by showing that fish spinal networks are fully equipped to control movements along more than just the axial plane.
Martha Bagnall, a post-doc in David McLean's lab at Northwestern University, USA, used whole-cell patch-clamp electrophysiology to record from primary motoneurons in the larval zebrafish spinal cord. By measuring the synchrony of input currents to pairs of motoneurons, she discovered that motoneurons that innervate dorsal and ventral muscles are driven by different premotor inputs. This surprising result means that motor circuits are organized in parallel, allowing independent control of muscles along both the anterior–posterior and dorsal–ventral axes.
The discovery of these parallel circuits in the fish spinal cord raised the possibility that movements could be initiated by differential activation of dorsal and ventral muscles within a single body quadrant. To test this hypothesis, Bagnall and McLean used calcium imaging to measure motoneuron activity when a fish rolled over, from a side-lounging position to a ready-to-swim stance. They observed that dorsal and ventral motoneurons were asymmetrically activated when the fish flipped. Further experiments showed that the descending input to motoneurons during flipping behavior depended on the vestibular system, which allows the fish to monitor self-motion and body orientation. However, the segregated organization of dorsal and ventral motoneurons remained whether or not the vestibular system was intact.
Together, these impressive electrophysiology and behavior experiments reveal a previously unappreciated level of intricacy in fish motor circuits. The authors suggest that fish spinal networks may have provided a template for the evolution of limb control circuits in tetrapods. It might be possible to shore up this idea by comparing the genes that specify development of fish dorsal and ventral motoneurons versus tetrapod flexor and extensor motoneurons. However, this theory is likely to remain on the bone-heap of speculation, as fish motoneurons are not well preserved in the fossil record.
Another important question raised by this study is the role that dorsal and ventral motoneurons play in fish rolling behavior. The authors show that dorsal and ventral motoneurons exhibit unequal activity when the fish rolls, but it is not clear whether this pattern of activity is really sufficient to cause the fish to flip over. Indeed, it is difficult to understand how simply flexing muscles on half the body would cause the animal to roll. It seems more likely that fish shift their weight or use their fins to generate torque, and, in the process, may asymmetrically activate dorsal and ventral motoneurons. Further work is needed to understand the biomechanics and neural control of this self-righting behavior. Fortunately, the ability to record from spinal circuits in behaving zebrafish provides a unique opportunity to investigate the interaction of multiple elements within an active motor circuit.
