In VivoImaging of Zebrafish Reveals Differences in the Spinal Networks for Escape and Swimming Movements

Abstract

Most studies of spinal interneurons in vertebrate motor circuits have focused on the activity of interneurons in a single motor behavior. As a result, relatively little is known about the extent to which particular classes of spinal interneurons participate in different behaviors. Similarities between the morphology and connections of interneurons activated in swimming and escape movements in different fish and amphibians led to the hypothesis that spinal interneurons might be shared by these behaviors. To test this hypothesis, we took advantage of the optical transparency of zebrafish larvae and developed a new preparation in which we could use confocal calcium imaging to monitor the activity of individual identified interneurons noninvasively, while we simultaneously filmed the movements of the fish with a high-speed digital camera. With this approach, we could directly examine the involvement of individual interneurons in different motor behaviors. Our work revealed unexpected differences in the interneurons activated in swimming and escape behaviors. The observations lead to predictions of different behavioral roles for particular classes of spinal interneurons that can eventually be tested directly in zebrafish by using laser ablations or mutant lines with interneuronal deficits.

Spinal Interneurons That Are Selectively Activated during Fictive Flexion Reflex

“…Moreover, the current results and a recent study in zebrafish (Ritter et al, 2001) both suggest that these shared and specialized subsets of spinal interneurons may to some extent be morphologically distinguishable. …”

Imaging Dedicated and Multifunctional Neural Circuits Generating Distinct Behaviors

“…Such an organization has been observed in locusts, in which two different interneuron pools that control walking and flight converge on the same (bifunctional) muscles (Ramirez and Pearson, 1988). In vivo calcium imaging experiments in zebrafish spinal cord have also demonstrated that two different sets of interneurons drive swimming and escape behaviors, suggesting that dedicated circuitry is also used by vertebrates (Ritter et al, 2001).…”

Anthropomorphism and ‘mental welfare’ of fishes

“…Sensory stimuli that elicit escape responses are diverse but typically abrupt, such as a looming visual stimulus, a sudden pulse of vibration, or sudden mechanical stimulus on the head or body (Grillner et al 1998, Bosch et al 2001, Ritter et al 2001, Rossignol et al 2006. These stimuli rapidly activate brainstem neurons, which excite spinal cord neurons that generate a rapid tail thrust.…”

“…These stimuli rapidly activate brainstem neurons, which excite spinal cord neurons that generate a rapid tail thrust. Activation of sustained swimming is produced by a network of spinal cord neurons known as the swimming pattern generator, which is regulated by neurons in the lower brainstem, that control the onset, offset, and speed of swimming (Grillner et al 1998, Ritter et al 2001, Rossignol et al 2006.…”