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Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network Dawn M

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Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network Dawn M Claremont Colleges Scholarship @ Claremont WM Keck Science Faculty Papers W.M. Keck Science Department 7-1-1999 Different Proctolin Neurons Elicit Distinct Motor Patterns From a Multifunctional Neuronal Network Dawn M. Blitz Miami University Andrew E. Christie Melissa J. Coleman Claremont McKenna College; Pitzer College; Scripps College Brian J. Norris Eve Marder Brandeis University See next page for additional authors Recommended Citation Blitz, Dawn M., Andrew E. Christie, Melissa J. Coleman, Brian J. Norris, Eve Marder, and Michael P. Nusbaum. "Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network." The ourJ nal of Neuroscience 19.13 (1999): 5449-5463. This Article is brought to you for free and open access by the W.M. Keck Science Department at Scholarship @ Claremont. It has been accepted for inclusion in WM Keck Science Faculty Papers by an authorized administrator of Scholarship @ Claremont. For more information, please contact [email protected]. Authors Dawn M. Blitz, Andrew E. Christie, Melissa J. Coleman, Brian J. Norris, Eve Marder, and Michael P. Nusbaum This article is available at Scholarship @ Claremont: http://scholarship.claremont.edu/wmkeckscience/40 The Journal of Neuroscience, July 1, 1999, 19(13):5449–5463 Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network Dawn M. Blitz,1 Andrew E. Christie,1,2 Melissa J. Coleman,1 Brian J. Norris,1 Eve Marder,2 and Michael P. Nusbaum1 1Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6074, and 2Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454 Distinct motor patterns are selected from a multifunctional tory commissural neuron 1 (MCN1) and the newly identified neuronal network by activation of different modulatory projec- modulatory commissural neuron 7 (MCN7). We document here tion neurons. Subsets of these projection neurons can contain that each of these neurons contains a unique complement of the same neuromodulator(s), yet little is known about the rela- cotransmitters and that each of these neurons elicits a distinct tive influence of such neurons on network activity. We have version of the pyloric motor pattern. Moreover, only one of them addressed this issue in the stomatogastric nervous system of (MCN1) also elicits a gastric mill rhythm. The MCN7-elicited the crab Cancer borealis. Within this system, there is a neuronal pyloric rhythm includes a pivotal switch by one STG network network in the stomatogastric ganglion (STG) that produces neuron from playing a minor to a major role in motor pattern many versions of the pyloric and gastric mill rhythms. These generation. Therefore, modulatory neurons that share a peptide different rhythms result from activation of different projection transmitter can elicit distinct motor patterns from a common neurons that innervate the STG from neighboring ganglia and target network. modulate STG network activity. Three pairs of these projection Key words: stomatogastric nervous system; crustacea; pro- neurons contain the neuropeptide proctolin. These include the jection neurons; neuromodulation; Cancer borealis; central pat- previously identified modulatory proctolin neuron and modula- tern generators Many neuronal networks produce multiple motor patterns Aston-Jones et al., 1996; Page and Sofroniew, 1996; Edwards and (Marder and Calabrese, 1996), in part because of activity of Kravitz, 1997; Jacobs and Fornal, 1997). different modulatory projection neurons (Norris et al., 1996; Projection neurons that share a neuromodulator might elicit Perrins and Weiss, 1996; Blitz and Nusbaum, 1997). However, in different responses from the same network because of the influ- many systems it is difficult to record from these neurons. Even in ence of distinct cotransmitters. The presence of cotransmitters is the systems in which such studies are undertaken, only some ubiquitous throughout all nervous systems (Weiss et al., 1993; projection neurons have had their transmitter(s) identified Lundberg, 1996; Brezina and Weiss, 1997). It is also possible that (Kuhlman et al., 1985; Nusbaum and Kristan, 1986; Nusbaum and a shared neuromodulator will affect a network in different ways Marder, 1989a; Thorogood and Brodfuehrer, 1995; Norekian and when released by distinct modulatory neurons, even in the ab- Satterlie, 1996; McCrohan and Croll, 1997). Consequently, little sence of different cotransmitters. For neuropeptide transmitters, is known about whether multiple projection neurons with a com- this could result from a compartmentalization of their actions, as mon modulatory transmitter influence a neural network in the would occur if their range of influence was limited by extracellu- same manner. Results from studies using exogenously applied lar peptidases (Sigvardt et al., 1986; Coleman et al., 1994; Saleh et neuromodulators, pharmacology, and/or stimulation of neuronal al., 1996) or if they were released either at different distances populations suggest a unified role for same transmitter-containing from their receptors or in different amounts (Vilim et al., 1996). neurons in their influence on network activity (McCormick, 1992; These issues can be studied in the crustacean stomatogastric nervous system (STNS) (Harris-Warrick et al., 1992a; Marder et al., 1997). This nervous system consists of the stomatogastric Received Feb. 17, 1999; revised April 8, 1999; accepted April 8, 1999. ganglion (STG), esophageal ganglion (OG) and commissural This work was supported by National Science Foundation Grants IBN94-96264 ganglia (CoGs), plus their connecting and motor nerves. Over- and IBN98-08356 (M.P.N.), National Institute of Neurological Disorders and Stroke lapping subsets of STG neurons generate the gastric mill and Grants NS29436 (M.P.N.), F32-NS09718 (A.E.C.), and NS17813 (E.M.), National Institute of Mental Health Training Grant MH-17168, and the Human Frontiers pyloric rhythms, which control the chewing and filtering behav- Science Program. We thank Drs. Debra Wood and David Perkel for advice on iors of the foregut, respectively (Weimann et al., 1991; Heinzel et statistical analysis and data presentation. al., 1993; Weimann and Marder, 1994). In the crab Cancer borea- Correspondence should be addressed to Dr. Michael P. Nusbaum, Department of Neuroscience, University of Pennsylvania School of Medicine, 215 Stemmler Hall, lis, ;20 pairs of projection neurons innervate the STG, most of Philadelphia, PA 19104-6074. which originate in the CoGs and OG (Coleman et al., 1992). Dr. Blitz’s present address: Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637. Here, we show that three modulatory projection neurons that Dr. Coleman’s present address: Division of Neurobiology, Barrow Neurological innervate the STG contain the same peptide transmitter, procto- Institute, St. Joseph’s Hospital, Phoenix, AZ 85013. lin, but each one has a distinct complement of cotransmitters. Dr. Norris’s present address: Biology Program, California State University, San Marcos, CA 92096. Moreover, under the same conditions, they each elicit distinct Copyright © 1999 Society for Neuroscience 0270-6474/99/195449-15$05.00/0 motor patterns from the STG neural network. This appears to 5450 J. Neurosci., July 1, 1999, 19(13):5449–5463 Blitz et al. • Distinct Rhythms from Different Proctolin Neurons result from the different cellular and synaptic mechanisms that The proctolinHA antibody labeling within the STNS is indistinguishable each proctolin neuron uses for motor pattern selection, including from that seen with the proctolinND and proctolinBO antibodies (A. E. Christie, D. M. Blitz, and M. P. Nusbaum, unpublished observations) their use of distinct cotransmitter complements. (Marder et al., 1986). Marder et al. (1986) showed that the proctolin Some of this work has appeared previously in abstract form immunoreactivity in the STNS is associated with a substance that is (Nusbaum et al., 1989; Christie et al., 1993; Coleman et al., 1993). chromatographically indistinguishable from native proctolin (amino acid sequence RYLPT). Tachykinin-related peptide (TRP) immunoreactiv- MATERIALS AND METHODS ity was examined using a rat monoclonal antibody generated against substance P (Accurate Chemicals, Westbury, NY) (Goldberg et al., 1988) Animals. Crabs, C. borealis, were obtained from commercial suppliers used at 1:300. This antibody cross-reacts with the native TRP in the crab (Boston, MA) and the Marine Biological Laboratory (Woods Hole, STNS, called C. borealis tachykinin-related peptide Ia (CabTRP Ia; MA). Animals were maintained in aerated artificial seawater at 10–12°C, APSGFLGMRamide) (Blitz et al., 1995; Christie et al., 1997a). GABA and were cold-anesthetized by packing in ice for 20–40 min before immunoreactivity was examined using a rabbit polyclonal antibody (Sig- dissection. The stomach, including the STNS, was removed from the ma) used at 1:200–1:500 (Christie, 1995). Preadsorption controls for animal, and the rest of the dissection was performed in chilled (;4°C) GABA immunolabeling in the STNS are described below. Two rabbit physiological saline. Data were obtained from 190 male crabs. polyclonal antibodies generated against FMRFamide were used, includ- Solutions. C. borealis physiological saline had the following composi- ing one from INCSTAR Corp. (Stillwater, MN) (Schmidt and Ache, tion (in mM): NaCl, 440; MgCl , 26; CaCl , 13; KCl, 11; Trizma base,
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