Interneuronal and Peptidergic Control of Motor Pattern Switching in<i>Aplysia</i>

Morgan, Peter T.; Jing, Jian; Vilim, Ferdinand S.; Weiss, Klaudiusz R.

doi:10.1152/jn.00438.2001

Cited by 97 publications

(258 citation statements)

References 63 publications

(59 reference statements)

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“…We used a system-oriented strategy that allowed us to identify and characterize a family of neuropeptides that induce rhythmic feeding motor output in Aplysia. This strategy took advantage of the fact that the CBCs fulfill a critical role in feeding behavior and that CBCs contain neuropeptides that act on the feeding circuitry (Sossin et al, 1987;Lloyd, 1989;Xin et al, 1999;Morgan et al, 2000Morgan et al, , 2002Jing and Weiss, 2001). MALDI analysis of the cut ends of the CBCs revealed a number of peaks, some of which are likely to represent novel peptides.…”

Section: Discussionmentioning

confidence: 99%

“…FCAPs-initiated buccal motor programs could be ingestive, egestive, or intermediate. Previous work has shown that neuropeptide APGWamide can bias motor programs toward ingestion Morgan et al, 2002), and neuropeptide ANPY can bias motor programs toward egestion (Kupfermann et al, 2001). Importantly, in contrast to the FCAPs, APGWamide and ANPY do not initiate motor programs.…”

Section: Discussionmentioning

confidence: 99%

“…12 A, B) (n ϭ 6 of 8). In the other two cases, the motor programs were either egestive (i.e., B8 fired mostly during protraction phase) or intermediate (i.e., B8 fired in both protraction and retraction) (Morgan et al, 2002). We also tested the effect of FCAPg and found that it can also induce multicycle motor programs; however, it is less potent than FCAPb.…”

Section: Physiological Action Of Fcapsmentioning

confidence: 99%

“…12 B, C). On the basis of the activity in the radula nerve or activity of B8 during protraction and retraction (Morton and Chiel, 1993a,b;Church and Lloyd, 1994;Nargeot et al, 1999;Jing and Weiss, 2001;Morgan et al, 2002), the motor programs elicited by FCAPb were ingestive (i.e., B8 fired most strongly during retraction phase) in a majority of preparations ( Fig. 12 A, B) (n ϭ 6 of 8).…”

Section: Physiological Action Of Fcapsmentioning

confidence: 99%

“…One of the preparations in which growing evidence indicates that peptidergic modulation plays an important role in initiation and regulation of behavior is Aplysia, in which neural circuits that mediate the consummatory phase of feeding behaviors are subject to extensive peptidergic modulation (Sossin et al, 1987;Xin et al, 1999;Morgan et al, 2000Morgan et al, , 2002Furukawa et al, 2001;Jing and Weiss, 2001). Previous work that has characterized some of the peptides in the feeding circuitry was performed on peptides that were originally identified from peripheral tissues or from other systems (Price and Greenberg, 1977;Morris et al, 1982;Cropper et al, 1987Cropper et al, , 1988.…”

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confidence: 99%

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

Sweedler

Rubakhin

et al. 2002

J. Neurosci.

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Physiological Action Of Fcapsmentioning

confidence: 99%

Section: Physiological Action Of Fcapsmentioning

confidence: 99%

mentioning

confidence: 99%

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

Sweedler

Rubakhin

et al. 2002

J. Neurosci.

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Localization of biogenic amines in the foregut of Aplysia californica: Catecholaminergic and serotonergic innervation

Martinez-Rubio

Serrano

2009

J of Comparative Neurology

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This study examined the catecholaminergic and serotonergic innervation of the foregut of Aplysia californica, a model system in which the control of feeding behaviors can be investigated at the cellular level. Similar numbers (15-25) of serotonin-like-immunoreactive (5HTli) and tyrosine hydroxylase-like-immunoreactive (THli) fibers were present in each (bilateral) esophageal nerve (En), the major source of pregastric neural innervation in this system. The majority of En 5HTli and THli fibers originated from the anterior branch (En2), which innervates the pharynx and the anterior esophagus. Fewer fibers were present in the posterior branch (En1), which innervates the majority of the esophagus and the crop. Backfills of the two En branches toward the central nervous system (CNS) labeled a single, centrifugally projecting serotonergic fiber, originating from the metacerebral cell (MCC). The MCC fiber projected only to En2. No central THli neurons were found to project to the En. Surveys of the pharynx and esophagus revealed major differences between their patterns of catecholaminergic (CA) and serotonergic innervation. Whereas THli fibers and cell bodies were distributed throughout the foregut, 5HTli fibers were present in restricted plexi, and no 5HTli somata were detected. Double-labeling experiments in the periphery revealed THli neurons projecting toward the buccal ganglion via En2. Other afferents received dense perisomatic serotonergic innervation. Finally, qualitative and quantitative differences were observed between the buccal motor programs (BMPs) produced by stimulation of the two En branches. These observations increase our understanding of aminergic contributions to the pregastric regulation of Aplysia feeding behaviors.

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Responses of cerebral GABA-containing CBM neuron to taste stimulation with seaweed extracts inAplysia kurodai

2005

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Aplysia kurodai distributed along Japan feeds well on Ulva pertusa but rejects Gelidium amansii with distinctive patterned movements of the jaws and radula. On the ventral side of the cerebral M cluster, four cell bodies of higher order neurons that send axons to the buccal ganglia are distributed (CBM neurons). We have previously shown that the dopaminergic CBM1 modulates basic feeding circuits in the buccal ganglia for rejection by firing at higher frequency after application of the aversive taste of seaweed such as Gelidium amansii. In the present experiments immunohistochemical techniques showed that the CBM3 exhibited gamma-aminobutyric acid (GABA)-like immunoreactivity. The CBM3 may be equivalent to the CBI-3 involved in changing the motor programs from rejection to ingestion in Aplysia californica. The responses of the CBM3 to taste stimulation of the lips with seaweed extracts were investigated by the use of calcium imaging. The calcium-sensitive dye, Calcium Green-1, was iontophoretically introduced into a cell body of the CBM3 using a microelectrode. Application of Ulva pertusa or Gelidium amansii extract induced different changes in fluorescence in the CBM3 cell body, indicating that taste of Ulva pertusa initially induced longer-lasting continuous spike responses at slightly higher frequency compared with that of Gelidium amansii. Considering a role of the CBM3 in the pattern selection, these results suggest that elongation of the initial firing response may be a major factor for the CBM3 to switch the buccal motor programs from rejection to ingestion after application of different tastes of seaweeds in Aplysia kurodai.

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Interneuronal and Peptidergic Control of Motor Pattern Switching inAplysia

Cited by 97 publications

References 63 publications

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

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

Localization of biogenic amines in the foregut of Aplysia californica: Catecholaminergic and serotonergic innervation

Responses of cerebral GABA-containing CBM neuron to taste stimulation with seaweed extracts inAplysia kurodai

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