Serotonin Enhances the Resistance Reflex of the Locomotor Network of the Crayfish through Multiple Modulatory Effects that Act Cooperatively

Abstract

Serotonin (5HT) is an endogenous amine that modifies posture in crustacea. Here, we examined the mechanisms of action of 5HT on the resistance reflex in crayfish legs. This reflex, which counteracts movements imposed on a limb, is based on a negative feedback system formed by proprioceptors that sense joint angle movements and activate opposing motoneurons. We performed intracellular recordings from depressor motoneurons while repetitively stretching and releasing a leg joint proprioceptor in a resting in vitro preparation (i.e., a preparation that lacks spontaneous rhythmic activity). 5HT increased the amplitude of the depolarization during the release phase of the proprioceptor (corresponding to an upward movement of the leg) and the discharge frequency of the motoneurons. The 5HT-induced increase in the resistance reflex is caused, to a large extent, by polysynaptic pathways because it was very attenuated in the presence of high divalent cation solution. In addition to this activation of the polysynaptic pathways, 5HT also has postsynaptic effects that enhance the resistance reflex. 5HT causes a tonic depolarization, as well as an increase in the time constant and input resistance of motoneurons. We developed a simple mathematical model to describe the integrative properties of the motoneurons. The conclusion of this study is that the input frequency and the decay time constant of the EPSPs interact in such a way that small simultaneous changes in these parameters can cause a large effect on summation. Therefore, the conjunction of presynaptic and postsynaptic changes produces a strong cooperative effect on the resistance reflex response.

Spatial segregation of excitatory and inhibitory effects of 5-HT on crayfish motoneurons

“…The same receptors are also near serotonergic terminals adjacent to the initial segment of LG (Edwards and Spitzer 2006). This receptor downregulates cAMP, which is consistent with inhibition (Araki et al 2005;Lee et al 2008).…”

“…In such experiments carried out on communal animals, two types of effects were observed: in some animals, bath application of 5-HT induced an increase of Dep MN excitability, whereas in others, 5-HT induced a decrease of excitability (Le Bon-Jego et al 2004). Here, in postural networks of isolated animals, we demonstrate that the increase and decrease of excitability involve different areas of the arbor of a given Dep MN.…”

“…In a previous paper (Le Bon-Jego et al 2004), it was shown that 5-HT modulates sensory-motor integration involved in postural control of crayfish walking legs via two main effects: altering R in of the Dep MN (i.e., its excitability) and controlling the polysynaptic sensory-motor pathway (i.e., its sensory synaptic input). In such experiments carried out on communal animals, two types of effects were observed: in some animals, bath application of 5-HT induced an increase of Dep MN excitability, whereas in others, 5-HT induced a decrease of excitability (Le Bon-Jego et al 2004).…”

“…By comparison with experiments using bath application of 5-HT (Cattaert et al 2010;Le Bon-Jego et al 2004), the pressure-evoked responses of 5-HT were fast (hyperpolarizing responses started in Ͻ500 ms after the onset of the pressure pulse when the pipette was correctly placed, see Fig. 3B, whereas depolarizing responses were observed in Ͻ2 s, Fig.…”

“…In crayfish, serotonin (5-HT) influences aggressiveness (Huber and Delago 1998;Huber et al 1997a,b), social status (Huber et al 1997b(Huber et al , 2001, and escape behavior (Teshiba et al 2001). At the cellular level, the effects of 5-HT depend on the animal's social history (Le Bon-Jego et al 2004;Yeh et al 1996Yeh et al , 1997 but also on the regimen of serotonin application in animals that have been socially isolated. In isolated animals, both a slowly applied high concentration (5 ϫ 10 Ϫ5 M) and a rapidly applied low concentration (10 Ϫ6 M) of 5-HT facilitate the synaptic response of the lateral giant escape command neurons (LGs), whereas a rapid application of the same concentration inhibits the response (Teshiba et al 2001;Yeh et al 1996Yeh et al , 1997.…”