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Peptidergic motoneurons in the buccal ganglia of Aplysia californica Immunocytochemical, morphological, and physiological characterizations

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Summary

We used physiological recordings, intracellular dye injections and immunocytochemistry to further identify and characterize neurons in the buccal ganglia of Aplysia calif ornica expressing Small Cardioactive Peptide-like immunoreactivity (SCP-LI). Neurons were identified based upon soma size and position, input from premotor cells B4 and B5, axonal projections, muscle innervation patterns, and neuromuscular synaptic properties. SCP-LI was observed in several large ventral neurons including B6, B7, B9, B10, and B11, groups of s1 and s2 cluster cells, at least one cell located at a branch point of buccal nerve n2, and the previously characterized neurons B1, B2 and B15.

B6, B7, B9, B10 and B11 are motoneurons to intrinsic muscles of the buccal mass, each displaying a unique innervation pattern and neuromuscular plasticity. Combined, these motoneurons innervate all major intrinsic buccal muscles (I1/I3, I2, I4, I5, I6). Correspondingly, SCP-LI processes were observed on all of these muscles. Innervation of multiple nonhomologous buccal muscles by individual motoneurons having extremely plastic neuromuscular synapses, represents a unique form of neuromuscular organization which is prevalent in this system. Our results show numerous SCPergic buccal motoneurons with widespread ganglionic processes and buccal muscle innervation, and support extensive use of SCPs in the control of feeding musculature.

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Abbreviations

SCP-LI :

small cardioactive peptide-like immunoreactivity

PSC :

postsynaptic current

EPSP :

excitatory postsynaptic potential

IPSP :

inhibitory postsynaptic potential

FI :

facilitation index

TMR :

time to maximal response

References

  • Abrams TW, Castellucci VF, Camarado JS, Kandel ER, Lloyd PE (1984) Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel. Proc Natl Acad Sci USA 81:7956–7960

    Google Scholar 

  • Alevizos A, Weiss KR, Koester J (1989) SCP-containing R20 neurons modulate respiratory pumping in Aplysia. J Neurosci 9(9): 3058–3071

    Google Scholar 

  • Atwood HL (1973) An attempt to account for the diversity of crustacean muscles. Am Zool 13:357–378

    Google Scholar 

  • Bishop CA, Wine JJ, O'Shea M (1984) Neuropeptide proctolin in postural motoneurons of the crayfish. J Neurosci 4(8): 2001–2009

    Google Scholar 

  • Calabrese RL (1989) Modulation of muscle and neuromuscular junctions in invertebrates. Semin The Neurosci 1:25–34

    Google Scholar 

  • Church PJ, Kirk MD (1988a) Identification and characterization of peptidergic motoneurons in the buccal ganglia of Aplysia californica using intracellular dye injections and immunocyto-chemistry. Biol Bull 175(2):315

    Google Scholar 

  • Church PJ, Kirk MD (1988b) Further localization of SCPBergic neurons in the buccal ganglia of Aplysia californica. Neurosci Abstr 14(1): 535

    Google Scholar 

  • Coates CJ, Bulloch AG (1985) Synaptic plasticity in the molluscan peripheral nervous system: physiology and role for peptides. J Neurosci 5(10): 2677–2684

    Google Scholar 

  • Cohen KP, Kirk MD (1990) Individual buccal motoneurons of Aplysia californica innervate multiple buccal muscles and display unique neuromuscular synaptic plasticities. Soc Neurosci Abstr 16:1227

    Google Scholar 

  • Cohen JL, Weiss KR, Kupfermann I (1978) Motor control of buccal muscles in Aplysia. J Neurophysiol 41:157–180

    Google Scholar 

  • Cropper EC, Lloyd PE, Reed W, Tenenbaum W, Kupfermann I, Weiss KR (1987a) Multiple neuropeptides in cholinergic motoneurons of Aplysia: Evidence for modulation intrinsic to the motor circuit. Proc Natl Acad Sci USA 84:3486–3490

    Google Scholar 

  • Cropper EC, Tenenbaum R, Kolks MAG, Kupfermann I, Weiss KR (1987b) Myomodulin: a bioactive neuropeptide present in an identified cholinergic buccal motor neuron of Aplysia. Proc Natl Acad Sci USA 84:5483–5486

    Google Scholar 

  • Cropper EC, Miller MW, Tenenbaum R, Kolks MAG, Kupfermann I, Weiss KR (1988) Structure and action of buccalin: a modulatory neuropeptide localized to an identified small cardioactive peptide-containing cholinergic motor neuron of Aplysia californica. Proc Natl Acad Sci USA 85:6177–6181

    Google Scholar 

  • Cropper EC, Price D, Tenenbaum R, Kupfermann I (1990) Release of peptide cotransmitters from a cholinergic motor neuron under physiological conditions. Proc Natl Acad Sci USA 87:933–937

    Google Scholar 

  • Fiore L, Meunier JM (1979) Synaptic connections and functional organization in Aplysia buccal ganglia. J Neurobiol 10(1):13–29

    Google Scholar 

  • Gardner D (1971) Bilateral symmetry and interneuronal organization in the buccal ganglia of Aplysia. Science 173:550–553

    Google Scholar 

  • Goldstein R, Kistler HB Jr., Steinbusch HWM, Schwartz JH (1984) Distribution of serotonin-immunoreactivity in juvenile Aplysia. J Neurosa 11:535–547

    Google Scholar 

  • Goldstein RS, Schwartz JH (1989) Catecholamine neurons in Aplysia: Improved light-microscope resolution and ultrastructural study using paraformaldehyde and glutaraldehyde (FaGlu) cytochemistry. J Neurobiol 20(4): 203–218

    Google Scholar 

  • Greenberg MJ, Price DA (1983) Invertebrate neuropeptide: native and naturalized. Annu Rev Physiol 45:271–288

    Google Scholar 

  • Hess SD, Prior DJ (1989) Small cardioactive peptide B modulates Limax feeding motoneurones. J Exp Biol 142:473–478

    Google Scholar 

  • Howells HH (1942) The structure and function of the alimentary canal of Aplysia punctata. Q J Microsc Sci 83:357–397

    Google Scholar 

  • Jan LY, Jan YN (1982) Peptidergic transmission in sympathetic ganglia of the frog. J Physiol (Lond) 327:219–246

    Google Scholar 

  • Kandel ER (1979) Behavioral biology of Aplysia. WH Freeman, San Fransisco CA

    Google Scholar 

  • Kirk MD (1989) Premotor neurons in the feeding system of Aplysia. J Neurobiol 20(5):497–512

    Google Scholar 

  • Kow LM, Pfaff DW (1988) Neuromodulatory actions of peptides. Annu Rev Pharmacol Toxicol 28:163–188

    Google Scholar 

  • Krieger DT (1983) Brain peptides: What, Where, Why? Science 222:975–985

    Google Scholar 

  • Kreiner T, Kirk MD, Scheller RH (1987) Cellular and synaptic morphology of a feeding motor circuit in Aplysia californica. J Comp Neurol 264(3): 311–325

    Google Scholar 

  • Kupfermann I (1974a) Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol 10:1–26

    Google Scholar 

  • Kupfermann I (1974b) Dissociation of the appetitive and consummatory phases of feeding behavior in Aplysia: a lesion study. Behav Biol 10:89–97

    Google Scholar 

  • Lehman HK, Price DA, Greenberg MJ (1984) The FMRFamide-like neuropeptide of Aplysia is FMRFamide. Biol Bull 167:460–466

    Google Scholar 

  • Lloyd PE (1988) Fast axonal transport of modulatory neuropeptides from central ganglia to components of the feeding system in Aplysia. J Neurosci 8(9): 3507–3514

    Google Scholar 

  • Lloyd PE, Willows AOD (1980) Identified peptidergic neurons activate the feeding motor program of Tritonia. Soc Neurosci Abstr 6:704

    Google Scholar 

  • Lloyd PE, Kupfermann I, Weiss KR (1984) Evidence for parallel actions of a molluscan neuropeptide and serotonin in mediating arousal in Aplysia. Proc Natl Acad Sci USA 81:2934–2937

    Google Scholar 

  • Lloyd PE, Mahon AC, Kupfermann I, Cohen JL, Scheller RH, Weiss KR (1985) Biochemical and immunocytochemical localization of molluscan small cardioactive peptides in the nervous system of Aplysia californica. J Neurosci 5:1851–1861

    Google Scholar 

  • Lloyd PE, Schacher S, Kupfermann I, Weiss KR (1986) Release of neuropeptides during intracellular stimulation of single identified Aplysia neurons in culture. Proc Natl Acad Sci USA 81:2934–2937

    Google Scholar 

  • Lloyd PE, Kupfermann I, Weiss KR (1987) Sequence of small cardioactive peptide a: a second member of a class of neuropeptides in Aplysia. Peptides 8:179–184

    Google Scholar 

  • Lloyd PE, Kupfermann I, Weiss KR (1988) Central peptidergic motoneurons regulate gut motility in Aplysia. J Neurophysiol 59(5):1613–1626

    Google Scholar 

  • Mahon AC, Lloyd PE, Weiss KR, Kupfermann I, Scheller RH (1985) The small cardioactive peptides a and b of Aplysia are derived from a common precursor molecule. Proc Natl Acad Sci USA 82:3925–3929

    Google Scholar 

  • Mayeri E, Rothman BS, Brownell PH, Branton WD, Padgett L (1985) Nonsynaptic characteristics of neurotransmission mediated by egg-laying hormone in the abdominal ganglion of Aplysia. J Neurosci 5:2060–2077

    Google Scholar 

  • McAllister LB, Scheller RH, Kandel ER, Axel R (1983) In situ hybridization to study the origin and fate of identified neurons. Science 222:800–808

    Google Scholar 

  • McCaman MW, Weinreich D, McCaman RE (1973) The determination of picomole levels of 5-HT and dopamine in Aplysia, Tritonia, and leech nervous tissues. Brain Res 53:129–137

    Google Scholar 

  • Miller MW, Kupfermann I, Weiss KR (1988) Characterization of SCPB immunoreactive cells in the buccal ganglion of Aplysia. Neurosci Abstr 14:536

    Google Scholar 

  • Morris HR, Panico M, Karplus A, Lloyd PE, Piniker B (1982) Ellucidation by FAB-MS of the structure of a new cardioactive peptide from Aplysia. Nature 300:643–645

    Google Scholar 

  • Murphy AD, Lukowiak K, Stell WK (1985) Peptidergic modulation of patterned motor activity in identified neurons in Helisoma. Proc Natl Acad Sci USA 82:7140–7144

    Google Scholar 

  • Nagahama T, Takata M (1988) Food-induced firing patterns in motoneurons producing jaw movements in Aplysia kurodai. J Comp Physiol A 162:729–738

    Google Scholar 

  • Ocorr KA, Byrne JH (1986) Evidence for separate receptors that mediate parallel effects of serotonin and small cardioactive peptide b (SCPb) on adenylate cyclase in Aplysia californica. Neurosci Lett 70:283–288

    Google Scholar 

  • Ono JK (1989) Synaptic connections in the buccal ganglia of Aplysia mediated by an identified neuron containing a CCK/gastrinlike peptide co-localized with acetylcholine. Brain Res 493:212–224

    Google Scholar 

  • O'Shea M, Schaefer M (1985) Neuropeptide function: the invertebrate contribution. Annu Rev Neurosci 8:171–198

    Google Scholar 

  • Plummer MR, Kirk MD (1990) Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: synaptic connections, effects on ongoing motor rhythms, and peptide modulation. J Neurophysiol 63(3): 539–558

    Google Scholar 

  • Price DA, Greenberg MJ (1977) The structure of a molluscan cardioexcitatory neuropeptide. Science 197:670–671

    Google Scholar 

  • Prior DJ, Watson WH (1988) The molluscan neuropeptide, SCPB, increases the responsiveness of the feeding motor program of Limax maximus. J Neurobiol 19:87–105

    Google Scholar 

  • Rathouz MM, Kirk MD (1988) Localization of catecholamines in the buccal ganglia of Aplysia californica. Brain Res 458:170–175

    Google Scholar 

  • Richmond JE, Murphy AD, Bulloch AGM, Lukowiak K (1986) Evidence for an excitatory effect of GABA on feeding patterned motor activity of Helisoma trivolvis. Neurosci Abstr 12:792

    Google Scholar 

  • Reed W, Weiss KR, Lloyd PE, Kupfermann I, Chen M, Bailey CH (1988) Association of neuroactive peptides with the protein secretory pathway in identified neurons of Aplysia californica: immunolocalization of SCPA and SCPB to the contents of dense-core vesicles and the trans face of the Golgi apparatus. J Comp Neurol 272:358–369

    Google Scholar 

  • Scott ML, Govind CK, Kirk MD (1991) Neuromuscular organization of the buccal system in Aplysia californica. J Comp Neurol (in press)

  • Shyamala M, Nambu JR, Scheller RH (1986) Expression of the egg-laying hormone gene family in the head ganglia of Aplysia. Brain Res 371:49–57

    Google Scholar 

  • Sossin WS, Kirk MD, Scheller RH (1987) Peptidergic modulation of neuronal circuitry controlling feeding in Aplysia. J Neurosci 7(3):671–681

    Google Scholar 

  • Strumwasser F (1967) Types of information stored in single neurons. In: Wiersma CAG (ed) Invertebrate nervous systems. Univ Chicago Press, Chicago, pp 291–319

    Google Scholar 

  • Susswein AJ, Kupfermann I, Weiss KR (1976) The stimulus control of biting in Aplysia. J Comp Physiol 108:75–96

    Google Scholar 

  • Susswein AJ, Weiss KR, Kupfermann I (1978) The effects of food arousal on the latency of biting in Aplysia. J Comp Physiol 123:31–41

    Google Scholar 

  • Taussig R, Sweetcordero A, Scheller RH (1989) Modulation of ionic currents in Aplysia motoneuron B15 by serotonin, neuropeptides and second messengers. J Neurosci 9(9): 3218–3229

    Google Scholar 

  • Weiss KR, Koch UT, Koester J, Rosen SC, Kupfermann I (1982) The role of arousal in modulating feeding behavior of Aplysia: neural and behavioral studies. In: Hoebel BG, Novin D (eds) The neural basis of feeding and reward. Haer Institute, Brunswick, ME, pp 25–57

    Google Scholar 

  • Weiss KR, Chiel HJ, Koch U, Kupfermann I (1986) Activity of an identified histaminergic neuron, and its possible role in arousal of feeding behavior in semi-intact Aplysia. J Neurosci 6(8): 2403–2415

    Google Scholar 

  • Whim MD, Lloyd PE (1989) Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia. Proc Natl Acad Sci USA 86:9034–9038

    Google Scholar 

  • Willows AOD, Lloyd PE, Masinovsky BP (1988) Multiple transmitter types in Trifonia. III. Modulation of central pattern generator controlling feeding. J Neurobiol 19:69–86

    Google Scholar 

  • Zoran MJ, Haydon PG, Matthews PJ (1989) Aminergic and peptidergic modulation of motor function at an identified neuromuscular junction in Helisoma. J Exp Biol 142:225–243

    Google Scholar 

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Author notes

  1. Paul J. Church

    Present address: Committee on Neurobiology, University of Chicago, 947 E. 58th St., 60637, Chicago, IL, USA

Authors and Affiliations

  1. University of Missouri-Columbia, Division of Biological Sciences, Lefevre Hall, 65211, Columbia, MO, USA

    Paul J. Church, Kevin P. Cohen, Marsha L. Scott & Mark D. Kirk

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Church, P.J., Cohen, K.P., Scott, M.L. et al. Peptidergic motoneurons in the buccal ganglia of Aplysia californica Immunocytochemical, morphological, and physiological characterizations. J Comp Physiol A 168, 323–336 (1991). https://doi.org/10.1007/BF00198352

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