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Different Roles for Homologous Interneurons in Species Exhibiting Similar Rhythmic Behaviors

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Different Roles for Homologous Interneurons in Species Exhibiting Similar Rhythmic Behaviors View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology 21, 1036–1043, June 21, 2011 ª2011 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2011.04.040 Report Different Roles for Homologous Interneurons in Species Exhibiting Similar Rhythmic Behaviors Akira Sakurai,1 James M. Newcomb,1,2 Joshua L. Lillvis,1 occur spontaneously or in response to electrical stimulation and Paul S. Katz1,* of a body wall nerve [2, 4, 5]. It had an average burst period of 1Neuroscience Institute, Georgia State University, 4.1 6 0.23 s (n = 25; see Figure 2A). In the isolated Dendronotus PO Box 5030, Atlanta, GA 30302, USA nervous system, analogous swim-like bursting activity, con- sisting of general alternation between the bursts in the left and right pedal ganglia, occurred spontaneously or in response Summary to body wall nerve stimulation. The average burst period in Dendronotus was 4.5 6 0.30 s (n = 13; see Figure 2D), which It is often assumed that similar behaviors in related species was not significantly different from that of the Melibe motor are produced by similar neural mechanisms. To test this, we pattern (p = 0.30, Student’s unpaired t test). Based on these examined the neuronal basis of a simple swimming behavior characteristics, we conclude that the bursting activity repre- in two nudibranchs (Mollusca, Opisthobranchia), Melibe sents the motor pattern underlying the Dendronotus swimming leonina and Dendronotus iris. The side-to-side swimming behavior. movements of Dendronotus [1] strongly resemble those of Melibe [2, 3]. In Melibe, it was previously shown that the Neuroanatomical Identification of Swim Interneuron 1 central pattern generator (CPG) for swimming is composed In Melibe, swim interneuron 1 (Si1Mel; http://neuronbank.org/ of two bilaterally symmetric pairs of identified interneurons, wiki/index.php/Si1) has particular anatomical characteristics swim interneuron 1 (Si1) and swim interneuron 2 (Si2), which that allow it to be unambiguously identified from animal to are electrically coupled ipsilaterally and mutually inhibit animal [2, 4]. There is a single Si1Mel soma on the dorsal both contralateral counterparts [2, 4]. We identified homo- surface of each of the paired cerebral ganglia (Figure 1A). logs of Si1 and Si2 in Dendronotus. (Henceforth, homolo- The Si1Mel soma is one of the largest in this region of the cere- gous neurons in each species will be distinguished by the bral ganglion and is clear of pigment. Intracellular fills with subscripts Den and Mel.) We found that Si2Den and Si2Mel Neurobiotin or biocytin showed that the axon makes a charac- play similar roles in generating the swim motor pattern. teristic posterior bend before projecting to the ipsilateral pedal However, unlike Si1Mel, Si1Den was not part of the swim ganglion (Figure 1B, arrowhead). We found that there were fine CPG, was not strongly coupled to the ipsilateral Si2Den, branches in the cerebral ganglion and longer, thicker branches and did not inhibit the contralateral neurons. Thus, species in the pedal ganglion. None of the branches were observed to differences exist in the neuronal organization of the swim exit body wall nerves, but in 8 of 16 Si1Mel neurons that were CPGs despite the similarity of the behaviors. Therefore, simi- examined, thin processes were seen in the thicker of the two larity in species-typical behavior is not necessarily predic- pedal commissures, which encircle the esophagus (PP2; tive of common neural mechanisms, even for homologous nomenclature according to [7]). neurons in closely related species. Combining intracellular Neurobiotin fills of Si1Mel with sero- tonin immunohistochemistry, we determined that the Si1Mel Results soma was always located near a set of previously identified serotonergic neurons, the CeSP neurons [7, 8] (ten Si1Mel Swimming Behaviors neurons in seven preparations) (Figure 1C, 5-HT). In addition Melibe leonina swims by flattening its body in the sagittal plane to their serotonin immunoreactivity, the CeSP neurons can and flexing from side to side [2–6] (see Figure S1A available be identified based on their electrophysiological properties online), repeatedly bending at the midpoint with a periodicity [8, 9], facilitating the identification of Si1Mel in living prepara- of 2–5 s (mean = 3.0 6 0.18 s, n = 18). This behavior can be tions by providing a landmark for locating the neuron. triggered when the foot is dislodged from the substrate or Another unique characteristic of Si1Mel is that it displayed when the body wall is contacted by a noxious stimulus, such FMRFamide-like immunoreactivity (Figure 1C, FMRFamide). as high-molarity salt solution [2, 3]. We observed that the Although this antiserum may be relatively nonspecific in that swimming behavior of Dendronotus iris occurred under the it might recognize more than the peptide FMRFamide, the same circumstances and resembled the Melibe swim (see staining pattern was very reproducible, allowing it to be used Figure S1B) with a periodicity of body flexions that ranged as a marker of cell types. In five preparations, all six Si1Mel from 2.0 to 4.4 s (mean = 2.9 6 0.14 s, n = 22). The two behav- neurons injected with either Neurobiotin or biocytin were iors were not statistically different (p = 0.53, Student’s found to double label with the antiserum against FMRFamide. unpaired t test). This suite of neuroanatomical characteristics uniquely defined Si1Mel, differentiating it from all other neurons in Melibe. In Dendronotus (Figure 1E), we found just one neuron in Fictive Swim Motor Patterns each half of the brain that shared all of the neuroanatomical In Melibe, the fictive motor pattern produced by the isolated characteristics of Si1 : a colorless, relatively large soma in nervous system, which underlies the swimming behavior, can Mel the cerebral ganglion, an ipsilaterally projecting axon with a characteristic bend near the soma (Figure 1F, arrowhead), 2Present address: Department of Biology, New England College, 98 Bridge and branching in the pedal ganglion that spread into PP2 Street, Henniker, NH 03242, USA (n = 17) (Figure 1F, arrows). To determine whether there were *Correspondence: [email protected] other neurons with this morphology, in 19 preparations, we Homologous Neurons and Similar Behaviors 1037 Figure 1. Comparison of the Neuroanatomy and Immunoreactivity of Swim Interneurons 1 and 2 in Melibe and Dendronotus (A and E) Schematic drawings of the Melibe brain (A) and the Dendronotus brain (E) showing cerebral, pleural, and pedal ganglia; the location of swim inter- neuron 1 (Si1, pink) and 2 (Si2, blue) somata and their neurites; and the locations of the serotonergic CeSP somata (green). The gross anatomy of the pedal ganglia in Dendronotus differs from that of Melibe in that the pedal ganglia are bilobed and the pedal commissures are much shorter than in Melibe.To encircle the esophagus, the distal lobes curl around the esophagus. (B and F) Neurobiotin fills of Si1 show the location of the soma in the cerebral ganglion of Melibe (B) and Dendronotus (F). The axon in both species has a characteristic posterior bend (arrowhead) before projecting to the ipsilateral pedal ganglion. (C and G) Left: Si1, labeled by intracellular injection of Neurobiotin (pink), is surrounded by the CeSP neurons (green), which are immunoreactive to serotonin (5-HT). Right: Si1, labeled by intracellular injection of Neurobiotin (pink), is doubled labeled (white) by antisera against the neuropeptide FMRFamide (green). (D and H) Both Si2Mel (D) and Si2Den (H) have a soma in the pedal ganglion and send a thick axon through the pedal commissure (PP2) to the opposite pedal ganglion, where they have a distinctive linearly shaped terminal arbor (arrows). injected a total of 43 neurons in this region with either Neuro- of this neuron was located near the serotonergic CeSP biotin or biocytin, and we did not see more than one neuron neurons (eleven neurons from eight preparations) (Figure 1G, on each side with this characteristic morphology. The soma 5-HT). Furthermore, in all six neurons in four preparations Current Biology Vol 21 No 12 1038 where it was examined, this neuron displayed FMRFamide-like A Melibe D Dendronotus immunoreactivity (Figure 1G, FMRFamide). On the basis of these properties, which uniquely define this neuron, we call it Si1Mel Si1Den 50 50 mV Si1Den and consider it a putative homolog of Si1Mel. (L) mV (L) Si1Den Identification of Swim Interneuron 2 Si1Mel 50 50 (R) mV In Melibe, there is a single swim interneuron 2 (Si2Mel; http:// (R) mV neuronbank.org/wiki/index.php/Si2) soma on the dorsal Si2 Si2 surface of each pedal ganglion [4]. Its axon projects to the Mel 50 Den 50 contralateral pedal ganglion through PP2 [4](Figures 1A and (R) mV (R) mV 1D). We found that Si2 had a characteristic linear, dense Mel PdGN arborization in the pedal ganglion (Figure 1D, arrows) (n = 4). 50 PdGN 50 mV We identified one neuron in Dendronotus in each side of the (L) (L) mV brain that shared similar anatomical characteristics to Si2Mel PdN2 PdN2 (n = 5) (Figures 1E and 1H). There was one soma on the dorsal (L) (R) surface of the proximal lobe of each pedal ganglion, which had 5 s 5 s an axon that projected through PP2 and terminated in the proximal lobe of the contralateral pedal ganglion. There, it BE had an axonal arborization similar to that of Si2Mel (Figure 1H, arrows). Based on these characteristics and the electrophysi- Si2Mel 50 Si2Den 50 mV mV ological characteristics (see below), we named this neuron (R) (R) 10 10 Si2Den and consider it a putative homolog of Si2Mel. nA nA Si2Mel Si2Den (L) 50 (L) 50 Si2Den but Not Si1Den Is a Member of the Swim Central mV mV Pattern Generator 5 s 5 s In Melibe, both Si1Mel and Si2Mel are core members of the swim central pattern generator (CPG), and both display bursting CF activity in phase with the swimming movements [2, 4].
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