Abstract
Dorsal Excitor motor neuron DE-3 in the medicinal leech plays three very different dynamical roles in three different behaviors. Without rewiring its anatomical connectivity, how can a motor neuron dynamically switch roles to play appropriate roles in various behaviors? We previously used voltage-sensitive dye imaging to record from DE-3 and most other neurons in the leech segmental ganglion during (fictive) swimming, crawling, and local-bend escape (Tomina and Wagenaar, 2017). Here, we repeated that experiment, then re-imaged the same ganglion using serial blockface electron microscopy and traced DE-3's processes. Further, we traced back the processes of DE-3's presynaptic partners to their respective somata. This allowed us to analyze the relationship between circuit anatomy and the activity patterns it sustains. We found that input synapses important for all the behaviors were widely distributed over DE-3's branches, yet that functional clusters were different during (fictive) swimming vs. crawling.
Highlights
Some neural circuits are responsible for only one specialized function
The nervous system of the leech comprises cephalic ganglia, a tail ganglion, and 21 nearly identical segmental ganglia connected by a ventral nerve cord (Muller et al, 1981; Wagenaar, 2015)
An individual segmental ganglion is a good stand-in for a whole nervous system, because its neurons capture the entire pathway from sensory input through self-generated interneuronal rhythms to motor output (Kristan et al, 2005), which is why we focused our imaging efforts there
Summary
Some neural circuits are responsible for only one specialized function. Examples include the exquisitely tuned delay lines that barn owls use to locate sounds (Carr and Konishi, 1988) and the motor neurons that control the honeybee’s stinger (Ogawa et al, 1995). In most animals’ central nervous systems, many circuits respond to stimuli of multiple sensory modalities or control more than one behavior (Briggman and Kristan, 2008). Motor cortex activity can be modulated not just by visual presentation of images of relevant body parts, but even in a working memory task in the absence of immediate stimuli (Galvez-Pol et al, 2018). All these forms of multifunctionality likely contribute to the versatility of large brains like ours and may help smaller animals use their more constrained neural hardware more efficiently (Briggman and Kristan, 2008)
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