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.
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
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
Alevizos A, Weiss KR, Koester J (1989 b) SCP-containing R20 neurons modulate respiratory pumping in Aplysia. J Neurosci 9:3058–3071
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
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
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
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
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
Arch S, Smock T (1977) Egg-laying behavior in Aplysia californica. Behav Biol 19:45–54
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
Barber A (1983) A monoamine-detecting histofluorescence technique for use on wholemounts of molluscan tissues. J Neurosci Meth 8:171–175
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
Buck LB, Bigelow JM, Axel R (1987) Alternative splicing in individual Aplysia neurons generates neuropeptide diversity. Cell 51:127–133
Byrne J, Koester J (1978) Respiratory pumping: neuronal control of a centrally commanded behavior in Aplysia. Brain 143:87–105
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
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
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
Dieringer N, Koester J, Weiss K (1978) Adaptive changes in heart rate of Aplysia californica. J Comp Physiol 123:11–21
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
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
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
Goldstein SR, Kistler HB, Steinbusch HWM, Schwartz JH (1984) Distribution of serotonin-immunoreactivity in juvenile Aplysia. Neuroscience 11:535–547
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
Hening WA (1982) Central generation and coordination of a complex behavioral sequence in Aplysia californica. PhD Dissertation, New York University, New York
Hening WA, Walters ET, Carew TJ, Kandel ER (1979) Motoneuronal control of locomotion in Aplysia. Brain Res 179:231–252
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
Kandel ER (1979) Behavioral biology of Aplysia. Freeman, San Francisco
Koch UT, Koester J (1982) Time sharing of heart power: cardiovascular adaptations to food-arousal in Aplysia. J Comp Physiol 149:31–42
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
Koester J, Koch UT (1987) Neural control of the circulatory system of Aplysia. Experientia 43:972–80
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
Kuslansky B, Weiss KR, Kupfermann I (1987) Mechanisms underlying satiation of feeding behavior of the mollusc Aplysia. Behav Neural Biol 48:278–303
Liebeswar G, Goldman JE, Koester J, Mayeri E (1975) Neural control of circulation in Aplysia III. Neurotransmitters. J Neurophysiol 38:767–779
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
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
Longley RD, Longley AJ (1986) Serotonin immunoreactivity of neurons in the gastropod Aplysia californica. J Neurobiol 17:339–358
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
Mayeri E, Koester J, Kupfermann I, Liebeswar G, Kandel ER (1974) Neural control of circulation in Aplysia. I. Motoneurons. J Neurophysiol 37:458–475
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
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
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
Sawada M, Blankenship JE, MCAdoo DJ (1981 b) Neural control of a molluscan blood vessel, anterior aorta of Aplysia. J Neurophysiol 46:967–986
Scott ML, Govind CK, Kirk MD (1991) Neuromuscular organization of the buccal system in Aplysia californica. J Comp Neurol 312:207–222
Segal MM, Koester J (1982) Convergent cholinergic neurons produce similar postsynaptic actions in Aplysia: Implications for neural organization. J Neurophysiol 47:742–759
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
Skelton ME, Buck LB, Koester J (1989) Innervation of the anterior arterial system of Aplysia californica. Soc Neurosci Abstr 15:1298
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
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
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
Walters ET, Erickson MT (1986) Directional control and the functional organization of defense responses in Aplysia. J Comp Physiol A 159:339–351
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
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
Author information
Authors and Affiliations
Rights 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
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00188923