{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,17]],"date-time":"2025-10-17T13:41:46Z","timestamp":1760708506299,"version":"3.41.2"},"reference-count":45,"publisher":"The Company of Biologists","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Summary<\/jats:title>\n               <jats:p>While many neurons are known to contain multiple neurotransmitters, the specific roles played by each co-transmitter within a neuron are often poorly understood. Here, we investigated the roles of the co-transmitters of the pyloric suppressor (PS) neurons, which are located in the stomatogastric nervous system (STNS) of the lobster, Homarus americanus. The PS neurons are known to contain histamine; using RT-PCR, we identified a second co-transmitter as the FMRFamide-like peptide crustacean myosuppressin (Crust-MS). The modulatory effects of Crust-MS application on the gastric mill and pyloric patterns, generated in the stomatogastric ganglion (STG), closely resembled those recorded following extracellular PS neuron stimulation. To determine whether histamine plays a role in mediating the effects of the PS neurons in the STG, we bath-applied histamine receptor antagonists to the ganglion. In the presence of the antagonists, the histamine response was blocked, but Crust-MS application and PS stimulation continued to modulate the gastric and pyloric patterns, suggesting that PS effects in the STG are mediated largely by Crust-MS. PS neuron stimulation also excited the oesophageal rhythm, produced in the commissural ganglia (CoGs) of the STNS. Application of histamine, but not Crust-MS, to the CoGs mimicked this effect. Histamine receptor antagonists blocked the ability of both histamine and PS stimulation to excite the oesophageal rhythm, providing strong evidence that the PS neurons use histamine in the CoGs to exert their effects. Overall, our data suggest that the PS neurons differentially utilize their co-transmitters in spatially distinct locations to coordinate the activity of three independent networks.<\/jats:p>","DOI":"10.1242\/jeb.082503","type":"journal-article","created":{"date-parts":[[2013,2,8]],"date-time":"2013-02-08T07:12:22Z","timestamp":1360307542000},"source":"Crossref","is-referenced-by-count":12,"title":["Coordination of distinct but interacting rhythmic motor programs by a modulatory projection neuron using different co-transmitters in different ganglia"],"prefix":"10.1242","author":[{"given":"Molly A.","family":"Kwiatkowski","sequence":"first","affiliation":[{"name":"Bowdoin College;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emily R.","family":"Gabranski","sequence":"additional","affiliation":[{"name":"Bowdoin College;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kristen E.","family":"Huber","sequence":"additional","affiliation":[{"name":"Bowdoin College;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"M. 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Biol."},{"key":"2021042507012829700_R2","doi-asserted-by":"crossref","first-page":"6774","DOI":"10.1523\/JNEUROSCI.19-16-06774.1999","article-title":"Distinct functions for cotransmitters mediating motor pattern selection","volume":"19","author":"Blitz","year":"1999","journal-title":"J. Neurosci."},{"key":"2021042507012829700_R3","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1017\/S0952523800005502","article-title":"Biochemical and physiological evidence that histamine is the transmitter of barnacle photoreceptors","volume":"3","author":"Callaway","year":"1989","journal-title":"Vis. Neurosci."},{"key":"2021042507012829700_R4","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/0304-3940(87)90394-6","article-title":"Suppressive control of a rhythmic central pattern generator by an identified modulatory neuron in Crustacea","volume":"81","author":"Cazalets","year":"1987","journal-title":"Neurosci. Lett."},{"key":"2021042507012829700_R5","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1523\/JNEUROSCI.10-02-00448.1990","article-title":"Suppressive control of the crustacean pyloric network by a pair of identified interneurons. I. Modulation of the motor pattern","volume":"10","author":"Cazalets","year":"1990","journal-title":"J. Neurosci."},{"key":"2021042507012829700_R6","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1523\/JNEUROSCI.10-02-00458.1990","article-title":"Suppressive control of the crustacean pyloric network by a pair of identified interneurons. II. Modulation of neuronal properties","volume":"10","author":"Cazalets","year":"1990","journal-title":"J. Neurosci."},{"key":"2021042507012829700_R7","doi-asserted-by":"crossref","first-page":"3962","DOI":"10.1242\/jeb.006577","article-title":"Histamine operates Cl-gated channels in crayfish neurosecretory cells","volume":"210","author":"Cebada","year":"2007","journal-title":"J. Exp. Biol."},{"key":"2021042507012829700_R8","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1002\/cne.11003","article-title":"Actions of a histaminergic\/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crab Cancer borealis","volume":"469","author":"Christie","year":"2004","journal-title":"J. Comp. Neurol."},{"key":"2021042507012829700_R9","doi-asserted-by":"crossref","first-page":"4135","DOI":"10.1007\/s00018-010-0482-8","article-title":"Crustacean neuropeptides","volume":"67","author":"Christie","year":"2010","journal-title":"Cell. Mol. Life Sci."},{"key":"2021042507012829700_R10","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1523\/JNEUROSCI.04-03-00708.1984","article-title":"Histamine as a neurotransmitter in the stomatogastric nervous system of the spiny lobster","volume":"4","author":"Claiborne","year":"1984","journal-title":"J. Neurosci."},{"key":"2021042507012829700_R11","first-page":"319","article-title":"Pharmacology and nerve-endings (Walter Ernest Dixon Memorial Lecture): (Section of Therapeutics and Pharmacology)","volume":"28","author":"Dale","year":"1935","journal-title":"Proc. R. Soc. Med."},{"key":"2021042507012829700_R12","doi-asserted-by":"crossref","first-page":"2278","DOI":"10.1242\/jeb.004770","article-title":"Identification and cardiotropic actions of sulfakinin peptides in the American lobster Homarus americanus","volume":"210","author":"Dickinson","year":"2007","journal-title":"J. Exp. Biol."},{"key":"2021042507012829700_R13","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1098\/rsnr.1976.0015","article-title":"From electrical to chemical transmission in the central nervous system","volume":"30","author":"Eccles","year":"1976","journal-title":"Notes Rec. R. Soc. Lond."},{"key":"2021042507012829700_R14","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1113\/jphysiol.1954.sp005226","article-title":"Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones","volume":"126","author":"Eccles","year":"1954","journal-title":"J. Physiol."},{"key":"2021042507012829700_R15","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1152\/jn.1994.71.3.1088","article-title":"Presynaptic inhibition is mediated by histamine and GABA in the crustacean escape reaction","volume":"71","author":"El Manira","year":"1994","journal-title":"J. Neurophysiol."},{"key":"2021042507012829700_R16","doi-asserted-by":"crossref","first-page":"2489","DOI":"10.1111\/j.1460-9568.2005.04442.x","article-title":"Reconfiguration of multiple motor networks by short- and long-term actions of an identified modulatory neuron","volume":"22","author":"Faumont","year":"2005","journal-title":"Eur. J. Neurosci."},{"key":"2021042507012829700_R17","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1002\/(SICI)1096-9861(19980928)399:3<289::AID-CNE1>3.0.CO;2-X","article-title":"Ontogenetic alteration in peptidergic expression within a stable neuronal population in lobster stomatogastric nervous system","volume":"399","author":"F\u00e9nelon","year":"1998","journal-title":"J. Comp. Neurol."},{"key":"2021042507012829700_R18","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.jphysparis.2003.10.007","article-title":"Maturation of rhythmic neural network: role of central modulatory inputs","volume":"97","author":"F\u00e9nelon","year":"2003","journal-title":"J. Physiol. Paris"},{"key":"2021042507012829700_R19","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1007\/s00359-004-0533-4","article-title":"Phylogenetic, ontogenetic and adult adaptive plasticity of rhythmic neural networks: a common neuromodulatory mechanism?","volume":"190","author":"F\u00e9nelon","year":"2004","journal-title":"J. Comp. Physiol. A"},{"key":"2021042507012829700_R20","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1002\/cne.903090308","article-title":"Single dopaminergic nigrostriatal neurons form two chemically distinct synaptic types: possible transmitter segregation within neurons","volume":"309","author":"Hattori","year":"1991","journal-title":"J. Comp. Neurol."},{"key":"2021042507012829700_R21","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1159\/000076158","article-title":"Crustacean motor pattern generator networks","volume":"13","author":"Hooper","year":"2004","journal-title":"Neurosignals"},{"key":"2021042507012829700_R22","doi-asserted-by":"crossref","first-page":"2108","DOI":"10.1242\/jeb.067603","article-title":"Targeting a neuropeptide to discrete regions of the motor arborizations of a single neuron","volume":"215","author":"Kueh","year":"2012","journal-title":"J. Exp. Biol."},{"key":"2021042507012829700_R23","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1152\/physrev.1991.71.3.683","article-title":"Functional studies of cotransmission","volume":"71","author":"Kupfermann","year":"1991","journal-title":"Physiol. Rev."},{"key":"2021042507012829700_R24","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1523\/JNEUROSCI.21-04-01313.2001","article-title":"Ontogeny of modulatory inputs to motor networks: early established projection and progressive neurotransmitter acquisition","volume":"21","author":"Le Feuvre","year":"2001","journal-title":"J. Neurosci."},{"key":"2021042507012829700_R25","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/j.ygcen.2008.01.009","article-title":"Mass spectral characterization of peptide transmitters\/hormones in the nervous system and neuroendocrine organs of the American lobster Homarus americanus","volume":"156","author":"Ma","year":"2008","journal-title":"Gen. Comp. Endocrinol."},{"key":"2021042507012829700_R26","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1146\/annurev.physiol.69.031905.161516","article-title":"Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs","volume":"69","author":"Marder","year":"2007","journal-title":"Annu. Rev. Physiol."},{"key":"2021042507012829700_R27","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/BF02331908","article-title":"Functional organization of cotransmission systems: lessons from small nervous systems","volume":"1","author":"Marder","year":"1995","journal-title":"Invert. Neurosci."},{"key":"2021042507012829700_R28","doi-asserted-by":"crossref","first-page":"1773","DOI":"10.1242\/jeb.054486","article-title":"Histaminergic signaling in the central nervous system of Daphnia and a role for it in the control of phototactic behavior","volume":"214","author":"McCoole","year":"2011","journal-title":"J. Exp. Biol."},{"key":"2021042507012829700_R29","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1038\/351060a0","article-title":"Construction of a pattern-generating circuit with neurons of different networks","volume":"351","author":"Meyrand","year":"1991","journal-title":"Nature"},{"key":"2021042507012829700_R30","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1523\/JNEUROSCI.14-02-00630.1994","article-title":"Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system","volume":"14","author":"Meyrand","year":"1994","journal-title":"J. Neurosci."},{"key":"2021042507012829700_R31","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1007\/BF00678725","article-title":"Neurons with histaminelike immunoreactivity in the segmental and stomatogastric nervous systems of the crayfish Pacifastacus leniusculus and the lobster Homarus americanus","volume":"266","author":"Mulloney","year":"1991","journal-title":"Cell Tissue Res."},{"key":"2021042507012829700_R32","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/s10158-009-0090-1","article-title":"Neuropeptide signaling near and far: how localized and timed is the action of neuropeptides in brain circuits?","volume":"9","author":"N\u00e4ssel","year":"2009","journal-title":"Invert. Neurosci."},{"key":"2021042507012829700_R33","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1038\/417343a","article-title":"A small-systems approach to motor pattern generation","volume":"417","author":"Nusbaum","year":"2002","journal-title":"Nature"},{"key":"2021042507012829700_R34","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/S0166-2236(00)01723-9","article-title":"The roles of co-transmission in neural network modulation","volume":"24","author":"Nusbaum","year":"2001","journal-title":"Trends Neurosci."},{"key":"2021042507012829700_R35","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1002\/syn.20300","article-title":"Choline acetyl transferase and neuropeptide immunoreactivities are colocalized in somata, but preferentially localized in distinct axon fibers and boutons of cat sympathetic preganglionic neurons","volume":"60","author":"S\u00e1mano","year":"2006","journal-title":"Synapse"},{"key":"2021042507012829700_R36","doi-asserted-by":"crossref","first-page":"2035","DOI":"10.1242\/jeb.204.12.2035","article-title":"Neuropeptides are ubiquitous chemical mediators: using the stomatogastric nervous system as a model system","volume":"204","author":"Skiebe","year":"2001","journal-title":"J. Exp. Biol."},{"key":"2021042507012829700_R37","doi-asserted-by":"crossref","first-page":"4845","DOI":"10.1073\/pnas.87.12.4845","article-title":"Dale's hypothesis revisited: different neuropeptides derived from a common prohormone are targeted to different processes","volume":"87","author":"Sossin","year":"1990","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042507012829700_R38","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1007\/s00359-009-0483-y","article-title":"Modulation of stomatogastric rhythms","volume":"195","author":"Stein","year":"2009","journal-title":"J. Comp. Physiol. A"},{"key":"2021042507012829700_R39","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.1016\/j.peptides.2007.08.019","article-title":"High-mass-resolution direct-tissue MALDI-FTMS reveals broad conservation of three neuropeptides (APSGFLGMRamide, GYRKPPFNGSIFamide and pQDLDHVFLRFamide) across members of seven decapod crustaean infraorders","volume":"28","author":"Stemmler","year":"2007","journal-title":"Peptides"},{"key":"2021042507012829700_R40","doi-asserted-by":"crossref","first-page":"3961","DOI":"10.1242\/jeb.035741","article-title":"The peptide hormone pQDLDHVFLRFamide (crustacean myosuppressin) modulates the Homarus americanus cardiac neuromuscular system at multiple sites","volume":"212","author":"Stevens","year":"2009","journal-title":"J. Exp. Biol."},{"key":"2021042507012829700_R41","doi-asserted-by":"crossref","first-page":"1874","DOI":"10.1523\/JNEUROSCI.22-05-01874.2002","article-title":"Colocalized neuropeptides activate a central pattern generator by acting on different circuit targets","volume":"22","author":"Thirumalai","year":"2002","journal-title":"J. Neurosci."},{"key":"2021042507012829700_R42","doi-asserted-by":"crossref","first-page":"3221","DOI":"10.1242\/jeb.200.24.3221","article-title":"FMRFamide-like peptides in the crayfish (Procambarus clarkii) stomatogastric nervous system: distribution and effects on the pyloric motor pattern","volume":"200","author":"Tierney","year":"1997","journal-title":"J. Exp. Biol."},{"key":"2021042507012829700_R43","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1002\/cne.902660103","article-title":"Purification and characterization of FMRFamidelike immunoreactive substances from the lobster nervous system: isolation and sequence analysis of two closely related peptides","volume":"266","author":"Trimmer","year":"1987","journal-title":"J. Comp. Neurol."},{"key":"2021042507012829700_R44","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1124\/mi.7.3.5","article-title":"On cotransmission and neurotransmitter phenotype plasticity","volume":"7","author":"Trudeau","year":"2007","journal-title":"Mol. Interv."},{"key":"2021042507012829700_R45","doi-asserted-by":"crossref","first-page":"9034","DOI":"10.1073\/pnas.86.22.9034","article-title":"Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia","volume":"86","author":"Whim","year":"1989","journal-title":"Proc. Natl. Acad. Sci. 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