Immunocytochemical mapping and quantification of expression of a putative type 1 serotonin receptor in the crayfish nervous system

Serotonin is an important neurotransmitter that is involved in modulation of sensory, motor, and higher functions in many species. In the crayfish, which has been developed as a model for nervous system function for over a century, serotonin modulates several identified circuits. Although the cellular and circuit effects of serotonin have been extensively studied, little is known about the receptors that mediate these signals. Physiological data indicate that identified crustacean cells and circuits are modulated via several different serotonin receptors. We describe the detailed immunocytochemical localization of the crustacean type 1 serotonin receptor, 5‐HT1crust, throughout the crayfish nerve cord and on abdominal superficial flexor muscles. 5‐HT1crust is widely distributed in somata, including those of several identified neurons, and neuropil, suggesting both synaptic and neurohormonal roles. Individual animals show very different levels of 5‐HT1crust immunoreactivity (5‐HT1crustir) ranging from preparations with hundreds of labeled cells per ganglion to some containing only a handful of 5‐HT1crustir cells in the entire nerve cord. The interanimal variability in 5‐HT1crustir is great, but individual nerve cords show a consistent level of labeling between ganglia. Quantitative RT‐PCR shows that 5‐HT1crust mRNA levels between animals are also variable but do not directly correlate with 5‐HT1crustir levels. Although there is no correlation of 5‐HT1crust expression with gender, social status, molting or feeding, dominant animals show significantly greater variability than subordinates. Functional analysis of 5‐HT1crust in combination with this immunocytochemical map will aid further understanding of this receptor's role in the actions of serotonin on identified circuits and cells. J. Comp. Neurol. 484:261–282, 2005. © 2005 Wiley‐Liss, Inc.

[1]  Distribution of GABAergic premotor nonspiking local interneurones in the terminal abdominal ganglion of the crayfish , 1997, The Journal of comparative neurology.

[2]  D. Kennedy,et al.  Cutaneous mechanoreceptors influencing motor output in the crayfish abdomen , 1967, Zeitschrift für vergleichende Physiologie.

[3]  E. S. Chang,et al.  Effects of exogenous serotonin on a motor behavior and shelter competition in juvenile lobsters (Homarus americanus) , 2000, Journal of Comparative Physiology A.

[4]  L. Mangiamele,et al.  Effects of serotonin and serotonin analogs on posture and agonistic behavior in crayfish , 2001, Journal of Comparative Physiology A.

[5]  E. Kravitz,et al.  The physiological properties of amine‐containing neurones in the lobster nervous system. , 1978, The Journal of physiology.

[6]  Crustacean Motor Neurons , 1977 .

[7]  RodrÍGuez-Sosa,et al.  Localization and release of 5-hydroxytryptamine in the crayfish eyestalk , 1997, The Journal of experimental biology.

[8]  Y. Kondoh,et al.  Neuroanatomy of the terminal (sixth abdominal) ganglion of the crayfish, Procambarus clarkii (Girard) , 1986, Cell and Tissue Research.

[9]  R. Harris-Warrick,et al.  Cellular mechanisms for modulation of posture by octopamine and serotonin in the lobster , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  R. Sandeman,et al.  Atlas of serotonin‐containing neurons in the optic lobes and brain of the crayfish, Cherax destructor , 1988, The Journal of comparative neurology.

[11]  R. Sullivan Stimulus-coupled 3H-serotonin release from identified neurosecretory fibers in the spiny lobster, Panulirus interruptus. , 1978, Life sciences.

[12]  D. H. Paul,et al.  Serotonergic and octopaminergic systems in the squat lobster Munida quadrispina (anomura, galatheidae) , 2001, The Journal of comparative neurology.

[13]  A. Tierney Structure and function of invertebrate 5-HT receptors: a review. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[14]  X. Langlois,et al.  Production and characterization of polyclonal antibodies recognizing the intracytoplasmic third loop of the 5-hydroxytryptamine1A receptor , 1994, Neuroscience.

[15]  F. Clarac,et al.  In vitro, protolin and serotonin induced modulations of the abdominal motor system activities in crayfish , 1993, Brain Research.

[16]  I. Cooke,et al.  6 – Hormones and Neurosecretion , 1982 .

[17]  B. Bush,et al.  Peripheral modulation of mechanosensitivity in primary afferent neurons , 1987, Nature.

[18]  R. Harris-Warrick Amine modulation of extension command element-evoked motor activity in the lobster abdomen , 1985, Journal of Comparative Physiology A.

[19]  Y. Kondoh,et al.  Intersegmental to intrasegmental conversion by ganglionic fusion in lateral giant interneurones of crayfish , 1983 .

[20]  F. Clarac,et al.  Central neuronal projections and neuromuscular organization of the basal region of the shore crab leg , 1983, The Journal of comparative neurology.

[21]  Mapping of serotonin-like immunoreactivity in the ventral nerve cord of crayfish , 1990, Brain Research.

[22]  Morphological and physiological characterization of individual olfactory interneurons connecting the brain and eyestalk ganglia of the crayfish , 1988, Journal of Comparative Physiology A.

[23]  C. McKittrick,et al.  Serotonin receptor binding in a colony model of chronic social stress , 1995, Biological Psychiatry.

[24]  F. Clarac,et al.  Neuromodulation of reciprocal glutamatergic inhibition between antagonistic motoneurons by 5-hydroxytryptamine (5-HT) in crayfish walking system , 1998, Neuroscience Letters.

[25]  R. Harris-Warrick,et al.  Serotonin and Octopamine Produce Opposite Postures in Lobsters , 1980, Science.

[26]  S. Harzsch,et al.  Serotonin-immunoreactive neurons in the ventral nerve cord of Crustacea: a character to study aspects of arthropod phylogeny. , 2000, Arthropod structure & development.

[27]  E. Escamilla-Chimal,et al.  Daily variations in crustacean hyperglycaemic hormone and serotonin immunoreactivity during the development of crayfish. , 2001, The Journal of experimental biology.

[28]  J. Dudel,et al.  Facilitatory effects of 5-hydroxy-tryptamine on the crayfish neuromuscular junction , 1965, Naunyn-Schmiedebergs Archiv für experimentelle Pathologie und Pharmakologie.

[29]  I. Panek,et al.  Distribution and function of GABAB receptors in spider peripheral mechanosensilla. , 2003, Journal of neurophysiology.

[30]  E. Florey,et al.  The effects of octopamine and other amines on the heart and on neuromuscular transmission in decapod crustaceans: further evidence for a role as neurohormone. , 1978, Comparative biochemistry and physiology. C: Comparative pharmacology.

[31]  S. Watson,et al.  Regulation of Serotonin1A, Glucocorticoid, and Mineralocorticoid Receptor in Rat and Human Hippocampus: Implications for the Neurobiology of Depression , 1998, Biological Psychiatry.

[32]  J John Mann,et al.  Role of the Serotonergic System in the Pathogenesis of Major Depression and Suicidal Behavior , 1999, Neuropsychopharmacology.

[33]  L. Fischer,et al.  Modulation of synaptic transmission and excitation-contraction coupling in the opener muscle of the crayfish, Astacus leptodactylus, by 5-hydroxytryptamine and octopamine. , 1983, The Journal of experimental biology.

[34]  Wilkens Possible mechanisms of control of vascular resistance in the lobster Homarus americanus , 1997, The Journal of experimental biology.

[35]  D. H. Edwards,et al.  Dual and Opposing Modulatory Effects of Serotonin on Crayfish Lateral Giant Escape Command Neurons , 2001, The Journal of Neuroscience.

[36]  Manfred Schmidt Continuous neurogenesis in the olfactory brain of adult shore crabs, Carcinus maenas , 1997, Brain Research.

[37]  E. Kravitz Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. , 1988, Science.

[38]  H. Fields,et al.  Reflex role played by efferent control of an invertebrate stretch receptor. , 1967, Journal of neurophysiology.

[39]  D. Dixon,et al.  Phosphatidylinositol system's role in serotonin-induced facilitation at the crayfish neuromuscular junction. , 1989, Journal of neurophysiology.

[40]  J. Bockaert,et al.  Distribution of metabotropic glutamate receptor DmGlu‐A in Drosophila melanogaster central nervous system , 2001, The Journal of comparative neurology.

[41]  D. H. Paul,et al.  Serotonin and octopamine elicit stereotypical agonistic behaviors in the squat lobster Munida quadrispina (Anomura, Galatheidae) , 1997, Journal of Comparative Physiology A.

[42]  Castanon-Cervantes,et al.  Rhythmic changes in the serotonin content of the brain and eyestalk of crayfish during development , 1999, The Journal of experimental biology.

[43]  E. Kravitz,et al.  Mapping of serotonin-like immunoreactivity in the lobster nervous system , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  E. Kravitz,et al.  Crustacean hyperglycemic hormone in the lobster nervous system: Localization and release from cells in the subesophageal ganglion and thoracic second roots , 1999, The Journal of comparative neurology.

[45]  R. Sandeman,et al.  Substance P antibody reveals homologous neurons with axon terminals among somata in the crayfish and crab brain , 1990, The Journal of comparative neurology.

[46]  V. Alones,et al.  Identification of three classes of multiglomerular, broad-spectrum neurons in the crayfish olfactory midbrain by correlated patterns of electrical activity and dendritic arborization , 1995, Journal of Comparative Physiology A.

[47]  R. Sandeman,et al.  Crayfish brain interneurons that converge with serotonin giant cells in accessory lobe glomeruli , 1995, The Journal of comparative neurology.

[48]  V. Alones,et al.  Anatomy and fine structure of neurons in the deutocerebral projection pathway of the crayfish olfactory system , 1992, The Journal of comparative neurology.

[49]  A. Mercer,et al.  Antennal lobe neurons of the honey bee, Apis mellifera, express a D2‐like dopamine receptor in vitro , 1997, The Journal of comparative neurology.

[50]  B. Beltz,et al.  Amines and peptides in the brain of the American lobster: immunocytochemical localization patterns and implications for brain function , 1997, Cell and Tissue Research.

[51]  B. Mulloney,et al.  GABA‐ergic neurons in the crayfish nervous system: An immunocytochemical census of the segmental ganglia and stomatogastric system , 1990, The Journal of comparative neurology.

[52]  V. M. Pasztor,et al.  THE MODULATORY EFFECTS OF SEROTONIN, NEUROPEPTIDE F1 AND PROCTOLIN ON THE RECEPTOR MUSCLES OF THE LOBSTER ABDOMINAL STRETCH RECEPTOR AND THEIR EXOSKELETAL MUSCLE HOMOLOGUES , 1993 .

[53]  D. H. Edwards,et al.  The Effect of Social Experience on Serotonergic Modulation of the Escape Circuit of Crayfish , 1996, Science.

[54]  R. Elson Neuroanatomy of a crayfish thoracic ganglion: Sensory and motor roots of the walking‐leg nerves and possible homologies with insects , 1996, The Journal of comparative neurology.

[55]  Christiane Rossi-Durand,et al.  Peripheral proprioceptive modulation in crayfish walking leg by serotonin , 1993, Brain Research.

[56]  U. García,et al.  Modulation of electrical activity by 5-hydroxytryptamine in crayfish neurosecretory cells. , 1997, The Journal of experimental biology.

[57]  R. Sandeman,et al.  Morphology of the Brain of Crayfish, Crabs, and Spiny Lobsters: A Common Nomenclature for Homologous Structures. , 1992, The Biological bulletin.

[58]  Chi-Ying Lee,et al.  Serotonergic Regulation of Crustacean Hyperglycemic Hormone Secretion in the Crayfish, Procambarus clarkii , 2001, Physiological and Biochemical Zoology.

[59]  D. H. Edwards,et al.  A crustacean serotonin receptor: Cloning and distribution in the thoracic ganglia of crayfish and freshwater prawn , 2004, The Journal of comparative neurology.

[60]  L. Lanfumey,et al.  Stress‐induced alterations of somatodendritic 5‐HT1A autoreceptor sensitivity in the rat dorsal raphe nucleus — in vitro electrophysiological evidence , 1997, Fundamental & clinical pharmacology.

[61]  R. Harris-Warrick,et al.  Multiple receptors mediate the modulatory effects of serotonergic neurons in a small neural network. , 1994, The Journal of experimental biology.

[62]  W. J. Heitler,et al.  Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish , 1999, Trends in Neurosciences.

[63]  B. Mulloney,et al.  Functional organization of crayfish abdominal ganglia. III. Swimmeret motor neurons , 2000, The Journal of comparative neurology.

[64]  Comparative Analysis of Neurogenesis in the Central Olfactory Pathway of Adult Decapod Crustaceans by In Vivo BrdU Labeling. , 1999, The Biological bulletin.

[65]  J. Wilkens The control of cardiac rhythmicity and of blood distribution in crustaceans , 1999 .

[66]  J. Hose,et al.  Chapter 17 – Circulation, the Blood, and Disease , 1995 .

[67]  E. Kravitz,et al.  Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior , 2000, Journal of Comparative Physiology A.

[68]  S. Shibata,et al.  Extended action of MKC‐242, a selective 5‐HT1A receptor agonist, on light‐induced Per gene expression in the suprachiasmatic nucleus in mice , 2002, Journal of neuroscience research.

[69]  E. Kravitz,et al.  Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[70]  L. Descarries,et al.  Somatodendritic localization of 5‐HT1A and preterminal axonal localization of 5‐HT1B serotonin receptors in adult rat brain , 2000, The Journal of comparative neurology.

[71]  Wilkens,et al.  Vascular peripheral resistance and compliance in the lobster Homarus americanus , 1997, The Journal of experimental biology.

[72]  R. Cooper,et al.  The effects of 5-HT on sensory, central and motor neurons driving the abdominal superficial flexor muscles in the crayfish. , 2000, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[73]  S R Yeh,et al.  Neuronal Adaptations to Changes in the Social Dominance Status of Crayfish , 1997, The Journal of Neuroscience.

[74]  M. P. Nusbaum,et al.  A small-systems approach to motor pattern generation , 2002, Nature.

[75]  D. H. Edwards,et al.  Parallel changes in agonistic and non-agonistic behaviors during dominance hierarchy formation in crayfish , 2003, Journal of Comparative Physiology A.

[76]  Daniel Cattaert,et al.  Serotonin Enhances the Resistance Reflex of the Locomotor Network of the Crayfish through Multiple Modulatory Effects that Act Cooperatively , 2004, The Journal of Neuroscience.

[77]  D. Baro,et al.  Arthropod 5-HT2 Receptors: A Neurohormonal Receptor in Decapod Crustaceans That Displays Agonist Independent Activity Resulting from an Evolutionary Alteration to the DRY Motif , 2004, The Journal of Neuroscience.

[78]  Serotonergic modulation of nonspiking local interneurones in the terminal abdominal ganglion of the crayfish. , 2002, The Journal of experimental biology.

[79]  A. Selverston,et al.  The stomatogastric nervous system: Structure and function of a small neural network , 1976, Progress in Neurobiology.

[80]  E. Meller,et al.  5-HT1A receptor-mediated regulation of mitogen-activated protein kinase phosphorylation in rat brain. , 2002, European journal of pharmacology.

[81]  B. Beltz,et al.  Serotonin Depletion In Vivo Inhibits the Branching of Olfactory Projection Neurons in the Lobster Deutocerebrum , 2000, The Journal of Neuroscience.

[82]  W. Huang,et al.  Serotonergic regulation of blood glucose levels in the crayfish, Procambarus clarkii: site of action and receptor characterization. , 2000, The Journal of experimental zoology.

[83]  M. Maclean,et al.  5‐hydroxytryptamine and the pulmonary circulation: receptors, transporters and relevance to pulmonary arterial hypertension , 2000, British journal of pharmacology.

[84]  B. Roth,et al.  Molecular biology of serotonin receptors structure and function at the molecular level. , 2002, Current topics in medicinal chemistry.

[85]  Fadi A. Issa,et al.  Dominance hierarchy formation in juvenile crayfish procambarus clarkii , 1999, The Journal of experimental biology.

[86]  A. Ramage Central cardiovascular regulation and 5-hydroxytryptamine receptors , 2001, Brain Research Bulletin.

[87]  F. Chaouloff,et al.  Serotonin and Stress , 1999, Neuropsychopharmacology.

[88]  B. Beltz,et al.  Effects of serotonin depletion on local interneurons in the developing olfactory pathway of lobsters. , 2001, Journal of neurobiology.