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Spinal cords and equivalent structures in invertebrates (nerve cords) often generate rhythmic motor patterns without inputs from sensory systems or the brain. Preparations that generate such ‘fictive rhythms’ have been used to uncover properties of motor circuits in many animals. The (largely untested) assumption has always been that circuits in these preparations are fundamentally the same with or without the brain. However, Olivia Mullins and Otto Friesen at the University of Virginia recently decided to see whether this assumption is true in the leech Hirudo verbena.

In previous work, Mullins and Friesen identified a neuron (E21) that, in the absence of the brain, appears to be a ‘command-like’ neuron. When stimulated, it initiates and enhances fictive swimming exclusively. The team wanted to see how E21's ability to drive swimming would be modulated when the brain was intact. To do this, they dissected out the brain and nerve cord and put them in a dish. Then they evoked fictive swim episodes by shocking a motor nerve. During swim bouts, they stimulated E21 and measured any resulting effects on fictive motor patterns. Surprisingly, the duo found that with the brain attached, E21's actions within the swim circuit were wildly variable. In some preparations, stimulating the cell enhanced fictive swimming, but in others, stimulation had no effect or exactly the opposite effect. The presence of the brain clearly added flexibility to what was thought at first to be a very rigid command circuit.

Leeches swim in water but crawl on land and the motor programs underlying each behavior are very different. The team wanted to see whether E21 activation can drive locomotor rhythms tailored for these two behavioral states. To this end, they kept the brain and anterior regions of the leech intact, while simultaneously recording from E21 and motor nerves involved in swimming. The front part of the leech was placed in sensory environments ranging from deep water (to enhance swimming) to solid substrate (to stimulate crawling). In the watery environment, E21 went back to enhancing swim episodes exclusively. But when the animal was faced with solid ground, E21 activation initiated and enhanced crawling. This suggests that instead of rigidly commanding downstream circuits to do a single behavior, E21 cells are commanding motor circuits to do an appropriate behavior based on sensory cues. This effect was completely masked in isolated preparations lacking brains.

How does the presence of the brain add flexibility to the circuits called into play by E21? The team measured how descending inputs from the brain affect the strength of a synapse between E21 and a downstream cell type known to ‘gate’ swimming. Gating cell activity is required to maintain swim episodes, so when the E21-to-gating cell synapse is weak, triggered swim episodes are shortened. In the absence of the brain, E21 strongly excites gating cells; however, when the brain is present, the connecting synapses are weaker and show increased variability. The mechanism remains mysterious, but it is possible that the modulation of this synapse by descending inputs accounts for much of the variability seen when E21 is stimulated in brain-attached preparations.

The work of Mullins and Friesen is important because it shows that a long-held assumption in motor systems research is not always true. Motor circuits can indeed be fundamentally different in the absence of the brain, and so we need to be careful how we interpret data from ‘brain-less’ preparations. Paradoxically, the team's work also highlights how useful it is to begin with such isolated preparations and then progressively add complexity back into them. At the end of the day, this simple approach may be the best way to really grasp how flexibility is generated in motor systems.

References

Mullins
O. J.
,
Friesen
W. O.
(
2012
)
The brain matters: effects of descending signals on motor control
.
J. Neurophysiol.
doi:
10.1152/jn.00107.2012
.