Modification of leech behavior patterns by reserpine-induced amine depletion

A single injection of 100 micrograms reserpine into the crop of the medicinal leech, Hirudo medicinalis, reduced CNS serotonin and dopamine levels to less than 1% of control values within 3 d. High-pressure liquid chromotography- (HPLC) determined CNS serotonin and dopamine levels remained maximally depressed for approximately 1 month following reserpine injection. Subsequently, amine levels recovered slowly, but remained depressed 6 months after reserpine injection. Following reserpine treatment, glyoxylic acid-induced fluorescence or neutral red staining closely mirrored the HPLC-determined time course of amine depletion and recovery. Acute exposure of isolated ganglia to 10 microM reserpine for periods up to 6 hr produced a 20–30% reduction of serotonin and dopamine content. The threshold concentration of reserpine necessary to produce amine depletion was approximately 1 microM. We found that reserpine treatment eliminated biting behavior within 4 d following injection. Biting behavior remained depressed below control levels for approximately 4 months, but returned to control values while CNS serotonin and dopamine levels remained significantly depressed at this time. Unexpectedly, reserpine treatment increased rather than reduced the duration of stimulus-evoked swimming activity. This behavioral change was evident within 3 d and persisted for approximately 3.5 months. To rapidly restore amine levels in reserpine-treated animals, we bathed intact leeches in pond water containing serotonin, dopamine, or octopamine. We found that biting behavior was restored following reserpine treatment by bathing intact leeches in pond water containing serotonin or dopamine, but not octopamine. Also contrary to expectations, the increase in swim duration was not reversed by bath exposure to serotonin, dopamine, octopamine, or histamine. However, all swimming activity in reserpine- treated leeches was eliminated by the amine antagonist cyproheptadine. We propose that the presence of low levels of amines is critical for the expression of both biting and swimming activity in leeches. However, the minimal levels of amines necessary for the expression of these behaviors are lower for swimming than for biting.

[1]  A. Carlsson.  FUNCTIONAL SIGNIFICANCE OF DRUG-INDUCED CHANGES IN BRAIN MONOAMINE LEVELS , 1964 .

[2]  R. Mccall,et al.  Fundamental statistics for psychology , 1972 .

[3]  Sten Grillner,et al.  On the Spinal Network Generating Locomotion in the Lamprey: Transmitters, Membrane Properties and Circuitry , 1986 .

[4]  E. Rosengren,et al.  TIME CORRELATION BETWEEN THE EFFECTS OF RESERPINE ON BEHAVIOUR AND STORAGE MECHANISM FOR ARYLALKYLAMINES. , 1963, Acta physiologica Scandinavica.

[5]  H. Horvitz,et al.  Serotonin and octopamine in the nematode Caenorhabditis elegans. , 1982, Science.

[6]  J. Belanger,et al.  Leydig cells: octopaminergic neurons in the leech , 1986, Brain Research.

[7]  P. A. Shore,et al.  The reserpine receptor. , 1978, Life sciences.

[8]  L. Murdock,et al.  Do plants psychomanipulate insects , 1985 .

[9]  G. Hoyle,et al.  Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. , 1984, Journal of neurobiology.

[10]  A. Dahlström,et al.  Recovery of noradrenaline in adrenergic axons of rat sciatic nerves after reserpine treatment , 1969, The Journal of pharmacy and pharmacology.

[11]  L. Murdock,et al.  Stimulation of blowfly feeding behavior by octopaminergic drugs. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Kammer,et al.  Octopamine and chlordimeform enhance sensory responsiveness and production of the flight motor pattern in developing and adult moths. , 1984, Journal of neurobiology.

[13]  C. Lent.  Serotonergic modulation of the feeding behavior of the medicinal leech , 1985, Brain Research Bulletin.

[14]  S. Grillner.  The Effect of L-DOPA on the Spinal Cord — Relation to Locomotion and the Half Center Hypothesis , 1986 .

[15]  N. J. Giarman,et al.  Drug-induced Changes in the Subcellular Distribution of Serotonin in Rat Brain with Special Reference to the Action of Reserpine , 1964 .

[16]  I. Orchard,et al.  Octopamine in leeches—I. Distribution of octopamine in Macrobdella decora and Erpobdella octoculata , 1980 .

[17]  B. Brodie,et al.  The role of brain serotonin in the mechanism of the central action of reserpine. , 1966, The Journal of pharmacology and experimental therapeutics.

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

[19]  J. Haeggendal,et al.  DISCLOSURE OF LABILE MONOAMINE FRACTIONS IN BRAIN AND THEIR CORRELATION TO BEHAVIOUR. , 1964, Acta physiologica Scandinavica.

[20]  M. Dickinson,et al.  Serotonin and Leech Feeding Behavior: Obligatory Neuromodulation , 1989 .

[21]  D. Njus,et al.  Multiple effects of reserpine on chromaffin-granule in membranes. , 1982, Biochemistry.

[22]  W. O. Friesen,et al.  Control of leech swimming activity by the cephalic ganglia. , 1986, Journal of neurobiology.

[23]  M H Dickinson,et al.  Ingestive behaviour and physiology of the medicinal leech. , 1988, The Journal of experimental biology.

[24]  A. Juorio,et al.  The Effect of Drugs on the Synthesis and Storage of Monoamines in Nervous Tissues of Molluscs , 1972 .

[25]  M. Lindqvist,et al.  Behavior and monoamine levels during long-term administration of reserpine to rabbits. , 1963, Acta physiologica Scandinavica.

[26]  M. Lindqvist,et al.  Further studies on monoamine metabolism and behaviour in rabbits chronically treated with reserpine. , 1967, Acta physiologica Scandinavica.

[27]  R. Johnson,et al.  Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. , 1988, Physiological reviews.

[28]  R. Coggeshall,et al.  The localization of 5‐hydroxytryptamine in chromaffin cells of the leech body wall , 1974, The Journal of comparative neurology.

[29]  W. Kristan,et al.  Swim initiation in the leech by serotonin-containing interneurones, cells 21 and 61. , 1986, The Journal of experimental biology.

[30]  G. A. Kerkut,et al.  Fluorescent microscopy of the 5HT- and catecholamine-containing cells in the central nervous system of the leech Hirudo medicinalis. , 1969, Comparative biochemistry and physiology.

[31]  A. Juorio.  Catecholamines and 5‐hydroxytryptamine in nervous tissue of cephalopods , 1971, The Journal of physiology.

[32]  J. Sladek,et al.  Dopamine cell replacement: Parkinson's disease. , 1990, Annual review of neuroscience.

[33]  M. Nusbaum.  Synaptic basis of swim initiation in the leech. III. Synaptic effects of serotonin-containing interneurones (cells 21 and 61) on swim CPG neurones (cells 18 and 208). , 1986, The Journal of experimental biology.

[34]  A. P. Kramer,et al.  Serotonin analog selectively ablates indentified neurons in the leech embryo. , 1982, Science.

[35]  L. Murdock,et al.  Amphetamine and Reserpine Deplete Brain Biogenic Amines and Alter Blow Fly Feeding Behavior , 1987, Journal of neurochemistry.

[36]  L. Murdock,et al.  Effects of substituted phenylethylamines on blowfly feeding behavior. , 1986, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.

[37]  V. Neuhoff,et al.  Tryptophan metabolism and the occurrence of amino acids and serotonin in the leech (Hirudo medicinalis) nervous system , 1976, Journal of neuroscience research.

[38]  R. Harris-Warrick,et al.  Amines and a peptide as neurohormones in lobsters: actions on neuromuscular preparations and preliminary behavioural studies. , 1980, The Journal of experimental biology.

[39]  W. O. Friesen,et al.  Modulation of swimming activity in the medicinal leech by serotonin and octopamine. , 1989, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.

[40]  R. Moore,et al.  Chapter 5 – Fluorescence Histochemistry , 1978 .

[41]  K. Ocorr,et al.  The identification and localization of a catecholamine in the motor neurons of the lobster cardiac ganglion. , 1983, Journal of neurobiology.

[42]  C. Lent.  Quantitative effects of a neurotoxin upon serotonin levels within tissue compartments of the medicinal leech. , 1984, Journal of neurobiology.

[43]  A. J. Sunderland,et al.  Evidence for an amine receptor on the Retzius cells of the leeches Hirudo Medicinalis and Haemopis Sanguisuga , 1980 .

[44]  H. Karten,et al.  IDENTIFICATION OF SEROTONIN WITHIN VITAL‐STAINED NEURONS FROM LEECH GANGLIA , 1979, Journal of neurochemistry.

[45]  B. D. Sloley,et al.  The effects of reserpine on amine concentrations in the nervous system of the cockroach (Periplaneta americana) , 1982 .

[46]  R. L. Mueller,et al.  Chromatographic and Histochemical Identification of Dopamine Within an Identified Neuron in the Leech Nervous System , 1983, Journal of neurochemistry.

[47]  P. A. Shore.  Release of serotonin and catecholamines by drugs. , 1962, Pharmacological reviews.