Modification of leech behavior patterns by reserpine-induced amine depletion

Abstract

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.

Dopamine and Glutamate Control Area-Restricted Search Behavior inCaenorhabditis elegans

“…Specific molecular mechanisms have not been reported for the control of these behaviors. However, there is substantial support for the dopaminergic control of feeding and search behaviors (O'Gara et al, 1991;Sawin et al, 2000;Foltin, 2001). Our results show how dopamine may regulate glutamatergic signaling in the locomotory control circuit to modulate turning in C. elegans and, therefore, generate a behavioral response to food deprivation.…”

“…ARS behavior is observed in a wide variety of animals (Bell, 1991), including house flies (White et al, 1984), leeches (O'Gara et al, 1991), moths (Vickers, 2000), populations of ladybug beetles (Kareiva and Odell, 1987), and rodents (Benedix, 1993). Specific molecular mechanisms have not been reported for the control of these behaviors.…”

A cephalic projection neuron involved in locomotion is dye coupled to the dopaminergic neural network in the medicinal leech

“…Such lesions may have led to a trauma-induced release of DA throughout the CNS. In a preliminary study, we pretreated several leeches with reserpine to eliminate the influence of endogenous DA (and other amines; O'Gara et al, 1991). In normal saline, we did indeed observe that the level of spontaneous fictive crawling was greatly reduced, further supporting a role for the amines.…”

“…The potential activation of the DA system by Tr2 may, in turn, help to coordinate locomotor activities with other behaviors. For example, dopaminergic innervation of the stomatogastric nervous system in the medicinal leech (Crisp et al, 2002) and other behavioral studies (O'Gara et al, 1991) suggest that DA may also regulate feeding-related behaviors. Possibly, DA suppresses swimming while coordinating the consumption of a blood meal, just as DA inhibits locomotion in the nematode Caenorhabditis elegans during encounters with food substrates, thus prolonging feeding (Horvitz et al, 1982;Sawin et al, 2000).…”

Beyond the central pattern generator: amine modulation of decision-making neural pathways descending from the brain of the medicinal leech

“…Only recently, however, have studies begun to examine the neuromodulation of command-like systems in the brain of the leech and how chemical modulation influences the initiation and termination of swimming (Crisp and Mesce, 2003;Crisp and Mesce, 2004). Such limited information contrasts with what has been accumulated at the level of the segmental swim circuits (Willard, 1981;Hashemzadeh-Gargari and Friesen, 1989;O'Gara et al, 1991;Angstadt and Friesen, 1993a;Angstadt and Friesen, 1993b;Mangan et al, 1994a;Mangan et al, 1994b;Mesce et al, 2001).…”