Skip to main content
Log in

The morphology, innervation and neural control of the anterior arterial system of Aplysia californica

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

The morphology, innervation, and neural control of the anterior arterial system of Aplysia californica were investigated. Immunocytochemical and histochemical techniques generated positive reactions in the anterior arterial system for several neuroactive substances, including SCPB, FMRFamide, R15α1 peptide, dopamine and serotonin. Three neurons were found to innervate the rostral portions of the anterior arterial tree. One is the identified peptidergic neuron R15 in the abdominal ganglion, and the other two are a pair of previously unidentified neurons, one in each pedal ganglion, named pedal arterial shorteners (PAS)- The endogeneously bursting neuron R15 was found to innervate the proximal anterior aorta. It also innervates a branch of the distal anterior aorta, the left pedal-parapodial artery. Activity in R15 causes constriction of the left pedal-parapodial artery. This effect is presumed to direct hemolymph towards the genital groove and penis on the right side in vivo. This vasoconstrictor action of R15 is mimicked by the R15α1 peptide. The PAS neuron pair causes longitudinal contraction of the rostral anterior aorta and the pedal-parapodial arteries. In vivo, the pair is active during behaviors involving head withdrawal and turning. By adjusting the length of the arteries during postural changes, the PAS neurons may prevent disturbances in blood flow due to bending or kinking of the arterial walls.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams WB, Benson JA (1985) The generation and modulation of endogenous rhythmicity in the Aplysia bursting pacemaker neurone R15. Prog Biophys Mol Biol 46:1–49

    Google Scholar 

  • Alevizos A, Bailey CH, Chen M, Koester J (1989 a) Innervation of vascular and cardiac muscle of Aplysia by multimodal motoneuron L7. J Neurophysiol 61:1053–1063

    Google Scholar 

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

    Google Scholar 

  • Alevizos A, Karagogeos D, Weiss KR, Buck L, Koester J (1991 a) R15α1 and R15α2 peptides from Aplysia: comparison of bioactivity, distribution and function of the two peptides generated by alternative splicing. J Neurobiol 22:405–417

    Google Scholar 

  • Alevizos A, Skelton M, Karagogeos D, Weiss KR, Koester J (1991) Physiological role of bursting neuron R15 of Aplysia in the control of egg laying behavior. In: Kits KS, Boer HH, Joose J (eds), Molluscan neurobiology. North Holland Publishing Company, Amsterdam, pp 61–66

    Google Scholar 

  • Alevizos A, Weiss KR, Koester J (1991 b) Synaptic actions of identified peptidergic neuron R15 in Aplysia. I. Activation of respiratory pumping. J Neurosci 11:1263–1274

    Google Scholar 

  • Alevizos A, Weiss KR, Koester J (1991 c) Synaptic actions of identified peptidergic neuron R15 in Aplysia. II. Contraction of pleuroabdominal connectives mediated by motoneuron L7. J Neurosci 11:1275–1281

    Google Scholar 

  • Alevizos A, Weiss KR, Koester J (1991 d) Synaptic actions of identified peptidergic neuron R15 in Aplysia. III. Activation of the large hermaphroditic duct. J Neurosci 11:1282–1290

    Google Scholar 

  • Arch S, Smock T (1977) Egg-laying behavior in Aplysia californica. Behav Biol 19:45–54

    Google Scholar 

  • Ascher P, Kehoe JS (1975) Amine and amino acid receptors in gastropod neurons. In: Iverson LL, Iverson SD, Snyder SH (eds) Handbook of psychopharmacology, vol 4. Plenum, New York, pp 265–310

    Google Scholar 

  • Barber A (1983) A monoamine-detecting histofluorescence technique for use on wholemounts of molluscan tissues. J Neurosci Meth 8:171–175

    Google Scholar 

  • Branton WD, Arch S, Smock T, Mayeri E (1978) Evidence for mediation of a neuronal interaction by a behaviorally active peptide. Proc Natl Acad Sci USA 75:5732–5736

    Google Scholar 

  • Buck LB, Bigelow JM, Axel R (1987) Alternative splicing in individual Aplysia neurons generates neuropeptide diversity. Cell 51:127–133

    Google Scholar 

  • Byrne J, Koester J (1978) Respiratory pumping: neuronal control of a centrally commanded behavior in Aplysia. Brain 143:87–105

    Google Scholar 

  • Carpenter D, Breese G, Schanberg S, Kopin I (1971) Serotonin and dopamine: distribution and accumulation in Aplysia nervous and non-nervous tissues. Int J Neurosci 2:49–56

    Google Scholar 

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

    Google Scholar 

  • De la Torre JC, Surgeon JW (1976) A methodological approach to rapid and sensitive monoamine histofluorescence using a modified glyoxylic acid technique: the SPG method. Histochemistry 49:81–93

    Google Scholar 

  • Dieringer N, Koester J, Weiss K (1978) Adaptive changes in heart rate of Aplysia californica. J Comp Physiol 123:11–21

    Google Scholar 

  • Dudek FE, Cobbs JS, Pinsker HM (1979) Bag cell electrical activity underlying spontaneous egg laying in freely behaving Aplysia brasiliana. J Neurophysiol 42:804–817

    Google Scholar 

  • Eales NB (1921) Aplysia. Liverpool Mar Biol Comm 1921, memoirs No. 24, pp 183–266

  • Ferguson GP, Ter Maat A, Parsons WD, Pinsker HM (1989) Egglaying in Aplysia. I. Behavioral patterns and muscle activity of freely behaving animals after selectively elicited bag cell discharges. J Comp Physiol A 164:835–847

    Google Scholar 

  • Goldstein RS (1984) Immunocytochemical, histofluorescent, and ultrastructural studies of monoaminergic neurons and their processes in Aplysia. PhD Dissertation, Columbia University

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

    Google Scholar 

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

    Google Scholar 

  • Hawkins RB (1989) Localization of potential serotonergic facilitator neurons in Aplysia by glyoxylic acid histofluorescence combined with retrograde fluorescent labeling. J Neurosci 9:4214–4226

    Google Scholar 

  • Hening WA (1982) Central generation and coordination of a complex behavioral sequence in Aplysia californica. PhD Dissertation, New York University, New York

    Google Scholar 

  • Hening WA, Walters ET, Carew TJ, Kandel ER (1979) Motoneuronal control of locomotion in Aplysia. Brain Res 179:231–252

    Google Scholar 

  • Hill RB (1964) Some effects of acetylcholine and of active amines on the isolated ventricles of Aplysia dactylomela and Aplysia fasciata. Pubbl Staz Zool Napoli 34:75–85

    Google Scholar 

  • Kandel ER (1979) Behavioral biology of Aplysia. Freeman, San Francisco

    Google Scholar 

  • Koch UT, Koester J (1982) Time sharing of heart power: cardiovascular adaptations to food-arousal in Aplysia. J Comp Physiol 149:31–42

    Google Scholar 

  • Koester J (1991) Identification of a network of neurons in the abdominal ganglion of Aplysia that are immunoreactive for the R15α peptides. Soc Neurosci Abstr 17:1355

    Google Scholar 

  • Koester J, Koch UT (1987) Neural control of the circulatory system of Aplysia. Experientia 43:972–80

    Google Scholar 

  • Kuramoto H, Yui R, Iwanaga T, Fujita T, Yanaihara N (1985) PHI-like immunoreactivity in the nervous system of the cockroach (insect) and Aplysia (mollusc) with special reference to its relationship to VIP-like immunoreactivity. Arch Histolog Jpn 48:427–433

    Google Scholar 

  • Kuslansky B, Weiss KR, Kupfermann I (1987) Mechanisms underlying satiation of feeding behavior of the mollusc Aplysia. Behav Neural Biol 48:278–303

    Google Scholar 

  • Liebeswar G, Goldman JE, Koester J, Mayeri E (1975) Neural control of circulation in Aplysia III. Neurotransmitters. J Neurophysiol 38:767–779

    Google Scholar 

  • Ligman SH, Brownell PH (1985) Differential hormonal action of the bag cell neurons on the arterial system of Aplysia. J Comp Physiol A 157:31–37

    Google Scholar 

  • Lloyd PE, Kupfermann I, Weiss KR (1985) Two endogenous neuropeptides (SCPA and SCPB) produce a cAMP-mediated stimulation of cardiac activity in Aplysia. J Comp Physiol A 156:659–667

    Google Scholar 

  • Longley RD, Longley AJ (1986) Serotonin immunoreactivity of neurons in the gastropod Aplysia californica. J Neurobiol 17:339–358

    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, Koester J, Kupfermann I, Liebeswar G, Kandel ER (1974) Neural control of circulation in Aplysia. I. Motoneurons. J Neurophysiol 37:458–475

    Google Scholar 

  • Miller MW, Alevizos A, Cropper EC, Vilim F., Karagogeos D, Kupfermann I, Weiss KR (1991) Localization of myomodulinlike immunoreactivity in the central nervous system and peripheral tissues of Aplysia californica. J Comp Neurol 313:1–8

    Google Scholar 

  • Miller MW, Alevizos A, Cropper EC, Kupfermann I, Weiss KR (1992) Localization of buccalin-like immunoreactivity in the central nervous system and peripheral tissues of Aplysia californica. J Comp Neurol (in press)

  • Rittenhouse AR, Price CH (1985) Peripheral axons of the parabolic burster neuron R15. Brain Res 333:330–335

    Google Scholar 

  • Sawada M, McAdoo DJ, Blankenship JE, Price CH (1981 a) Modulation of arterial muscle contraction in Aplysia by glycine and neuron R14. Brain Res 207:486–490

    Google Scholar 

  • Sawada M, Blankenship JE, MCAdoo DJ (1981 b) Neural control of a molluscan blood vessel, anterior aorta of Aplysia. J Neurophysiol 46:967–986

    Google Scholar 

  • Scott ML, Govind CK, Kirk MD (1991) Neuromuscular organization of the buccal system in Aplysia californica. J Comp Neurol 312:207–222

    Google Scholar 

  • Segal MM, Koester J (1982) Convergent cholinergic neurons produce similar postsynaptic actions in Aplysia: Implications for neural organization. J Neurophysiol 47:742–759

    Google Scholar 

  • Skelton ME, Koester J (1991) Innervation of the heart of Aplysia by serotonin and R15α1 peptide-immunoreactive terminals, and by neuron L2. Soc Neurosci Abstr 17:1355

    Google Scholar 

  • Skelton ME, Buck LB, Koester J (1989) Innervation of the anterior arterial system of Aplysia californica. Soc Neurosci Abstr 15:1298

    Google Scholar 

  • Taussig R, Kaldany RR, Rothbard JB, Schoolnik G, Scheller R (1985) Expression of the L11 neuropeptide gene in the Aplysia central nervous system. J Comp Neurol 238:53–64

    Google Scholar 

  • Teyke T, Weiss KR, Kupfermann I (1990) Appetitive feeding behavior of Aplysia: behavioral and neural analysis of directed head turning. J Neurosci 10:3922–3934

    Google Scholar 

  • Tritt SH, Lowe IP, Byrne JH (1983) A modification of the glyoxilic acid induced histofluorescence technique for demonstration of catecholamines and serotonin in tissues of Aplysia californica. Brain Res 259:159–162

    Google Scholar 

  • Walters ET, Erickson MT (1986) Directional control and the functional organization of defense responses in Aplysia. J Comp Physiol A 159:339–351

    Google Scholar 

  • Weiss KR, Bayley H, Lloyd PE, Tenenbaum R, Gawinowicz-Kolks MA, Buck L, Cropper E, Rosen SC, Kupfermann I (1989) Purification and sequencing of neuropeptides contained in neuron R15 of Aplysia californica. Proc Natl Acad Sci USA 86:2913–2917

    Google Scholar 

  • Winkler LR (1957) The biology of California sea hares of the genus Aplysia. PhD Dissertation University of Southern California

  • Wright DL (1960) Cardiac studies on Aplysia vaccaria. PhD Dissertation University of California, Los Angeles

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Skelton, M.E., Koester, J. The morphology, innervation and neural control of the anterior arterial system of Aplysia californica . J Comp Physiol A 171, 141–155 (1992). https://doi.org/10.1007/BF00188923

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00188923

Key words

Navigation