Functional organization of cotransmission systems: Lessons from small nervous systems

Marder, Eve; Christie, Andrew E.; Kilman, Valerie L.

doi:10.1007/bf02331908

Cited by 74 publications

(61 citation statements)

References 35 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…At least three possibilities exist. First, consistent with Dale's principle (Dale, 1935;Eccles et al, 1954;Eccles, 1976), the PS neurons might release histamine and Crust-MS equally at all terminals, but receptors could be differentially distributed (Marder et al, 1995). Second, the two co-transmitters might be present in the same terminals but released separately in response to different activity patterns (Whim and Lloyd, 1989).…”

Section: Discussionmentioning

confidence: 70%

“…While this may be true for some neurons, others are clearly capable of differentially packaging and trafficking neuroactive compounds to distinct compartments (Sossin et al, 1990;Hattori et al, 1991;Sámano et al, 2006;Kueh and Jellies, 2012) and/or differentially releasing co-transmitters in response to different activity patterns (Whim and Lloyd, 1989). Even when coreleased, co-transmitter actions can be compartmentalized via the differential distribution of their receptors (Marder et al, 1995;Thurimulai and Marder, 2002).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Coordination of distinct but interacting rhythmic motor programs by a modulatory projection neuron using different co-transmitters in different ganglia

Kwiatkowski

Gabranski

Huber

et al. 2013

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

SUMMARYWhile 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 cotransmitters in spatially distinct locations to coordinate the activity of three independent networks.

show abstract

Section: Discussionmentioning

confidence: 70%

Section: Introductionmentioning

confidence: 99%

Coordination of distinct but interacting rhythmic motor programs by a modulatory projection neuron using different co-transmitters in different ganglia

Kwiatkowski

Gabranski

Huber

et al. 2013

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

show abstract

“…Although extensive neuroanatomical and immunocytochemical work has demonstrated complex and rich patterns of colocalization for amines and peptides, how these substances modulate specific functional circuits remains relatively unknown. The stomatogastric nervous system contains ϳ20 different identified modulatory substances (Marder and Weimann, 1992;Marder et al, 1995;Christie et al, 1997a;Abbott and Marder, 1998), each of which can alter the STG motor patterns. The effects of serotonin (Kiehn and HarrisWarrick, 1992a,b;Zhang and Harris-Warrick, 1995), dopamine (Harris-Warrick et al, 1995a,b;Kloppenburg et al, 1999), and the peptide proctolin (Golowasch and Marder, 1992) have been characterized, but until now, the biophysical actions of most of the modulatory substances found in inputs to the STG were unknown.…”

Section: Discussionmentioning

confidence: 99%

“…The pyloric and gastric mill rhythms are modulated by a large number of peptides and amines that are present as circulating hormones and/or are released from modulatory projection and sensory neurons (Marder, 1987;Harris-Warrick et al, 1992;Christie et al, 1995;Marder et al, 1995;Marder and Calabrese, 1996). Despite the extensive study of the effects of modulators on the STG motor patterns (Marder and Calabrese, 1996;Marder et al, 2000) only proctolin and the amines have been studied with voltage-clamp methods.…”

mentioning

confidence: 99%

Multiple Peptides Converge to Activate the Same Voltage-Dependent Current in a Central Pattern-Generating Circuit

2000

Self Cite

View full text Add to dashboard Cite

The stomatogastric ganglion of the crab, Cancer borealis, is modulated by Ͼ20 different substances, including numerous neuropeptides. One of these peptides, proctolin, activates an inward current that shows strong outward rectification (Golowasch and Marder, 1992). Decreasing the extracellular Ca 2ϩ concentration linearizes the current-voltage curve of the proctolin-induced current. We used voltage clamp to study the currents evoked by proctolin and five additional modulators [C. borealis tachykinin-related peptide Ia (CabTRP Ia), crustacean cardioactive peptide, red pigment-concentrating hormone, TNRNFLRFamide, and the muscarinic agonist pilocarpine] in stomatogastric ganglion neurons, both in the intact ganglion and in dissociated cell culture. Subtraction currents yielded proctolinlike current-voltage relationships for all six substances, and the current-voltage curves of all six substances showed linearization in low external Ca 2ϩ . The lateral pyloric neuron responded to all six modulators, but the ventricular dilator neuron only responded to a subset of them. Bath application of saturating concentrations of proctolin occluded the response to CabTRP and vice versa. N-(6-Aminohexyl)-5-chloro-1-napthalensulfonamide, a calmodulin inhibitor, increased the amplitude and altered the voltage dependence of the responses elicited by CabTRP and proctolin. Together, these data indicate that all six substances converge onto the same voltage-dependent current, although they activate different receptors. Therefore, differential network responses evoked by these substances may primarily depend on the receptor distribution on network neurons.Key words: stomatogastric ganglion; crab; Cancer borealis; proctolin; CCAP; RPCH; crab tachykinin-related peptide; FLRFamide-related peptides Nervous systems contain many neuropeptides and amines that modulate synaptic strength and cellular excitability (Nicoll et al., 1990;Kupfermann, 1991;Marder and Calabrese, 1996;Marder, 1998). Most voltage-dependent ion channels are subject to modulation by one or more substances, and many agonists modulate multiple membrane currents (Kaczmarek and Levitan, 1987;Levitan, 1988Levitan, , 1994 Hille, 1992Hille, , 1994Gudermann et al., 1997). In principle, the large number of different intrinsic and synaptic currents subject to modulation could provide the potential substrate for virtually infinite modifications of circuit behavior under different modulatory conditions. Nonetheless, there are numerous examples of convergent actions of modulators, in which several substances act on the same current (Dunlap and Fischbach, 1978;Jones, 1985;Christie and North, 1988;Nicoll et al., 1990;Bolshakov et al., 1993; Brezina et al., 1994a,b;van Tol-Steye et al., 1997;Sodickson and Bean, 1998). Convergent actions of modulators may appear to be redundant at the level of the single neuron but may not be redundant at the level of network behavior, if different substances activate different receptors on separate populations of target neurons.The crustacean stomatogast...

show abstract

“…Because of several technical advantages of invertebrate nervous systems, these models systems are used extensively to gain insights into possible functions that neuropeptides play in feeding. Extensive research suggesting that peptides contribute to the functioning of neural circuits has been performed on invertebrate systems (Marder et al, 1995;Brezina and Weiss, 1997). Although many invertebrate neural circuits consist of a small number of neurons, such circuits are by no means simple in terms of cellular and molecular organization.…”

Section: Discussionmentioning

confidence: 99%

Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

Sweedler

Rubakhin

et al. 2002

J. Neurosci.

View full text Add to dashboard Cite

We use a multidisciplinary approach to identify, map, and characterize the bioactivity of modulatory neuropeptides in the circuitry that generates feeding behavior in Aplysia. Matrixassisted laser desorption/ionization time-of-flight mass spectrometry of the cerebral-buccal connective (CBC), a nerve containing axons of many interneurons that control feeding behavior of Aplysia, was used to identify neuropeptides that may participate in generation and shaping of feeding motor programs. Using this functionally oriented search, we identified a novel family of peptides that we call the feeding circuitactivating peptides (FCAPs). Two peptides with masses identical to those observed in the CBCs (molecular weight 1387 and 1433) were purified from buccal ganglia and partially sequenced using mass spectrometry. The amino acid sequence was then used to clone the FCAP precursor, which encodes multiple copies of eight different FCAPs. The two FCAPs present in highest copy number correspond to those observed in the CBC. The distribution of FCAP expression was mapped using Northern analysis, whole-mount in situ hybridization, and immunocytochemistry. Consistent with our initial findings, FCAP-immunopositive axons were observed in the CBC. Furthermore, we found that FCAP was present in some cerebralbuccal and buccal-cerebral interneurons. As their name suggests, FCAPs are capable of initiating rhythmic feeding motor programs and are the first neuropeptides with such activity in this circuit. The actions of FCAPs suggest that these peptides may contribute to the induction and maintenance of foodinduced arousal. FCAPs were also localized to several other neuronal systems, suggesting that FCAPs may play a role in the regulation of multiple behaviors.

show abstract

Functional organization of cotransmission systems: Lessons from small nervous systems

Cited by 74 publications

References 35 publications

Coordination of distinct but interacting rhythmic motor programs by a modulatory projection neuron using different co-transmitters in different ganglia

Coordination of distinct but interacting rhythmic motor programs by a modulatory projection neuron using different co-transmitters in different ganglia

Multiple Peptides Converge to Activate the Same Voltage-Dependent Current in a Central Pattern-Generating Circuit

Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

Contact Info

Product

Resources

About