Peripheral proprioceptive modulation in crayfish walking leg by serotonin

The social rank of an animal is distinguished by its behavior relative to others in its community. Although social-status-dependent differences in behavior must arise because of differences in neural function, status-dependent differences in the underlying neural circuitry have only begun to be described. We report that dominant and subordinate crayfish differ in their behavioral orienting response to an unexpected unilateral touch, and that these differences correlate with functional differences in local neural circuits that mediate the responses. The behavioral differences correlate with simultaneously recorded differences in leg depressor muscle EMGs and with differences in the responses of depressor motor neurons recorded in reduced, in vitro preparations from the same animals. The responses of local serotonergic interneurons to unilateral stimuli displayed the same status-dependent differences as the depressor motor neurons. These results indicate that the circuits and their intrinsic serotonergic modulatory components are configured differently according to social status, and that these differences do not depend on a continuous descending signal from higher centers.

Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 99%

Neural Circuit Reconfiguration by Social Status

Issa¹,

Drummond²,

Cattaert³

et al. 2012

“…In such preparations, MNs generally display passive properties: their VI curve is linear (at least in the range of a few millivolts from their resting potential) (Le Ray et al, 1997a). On these preparations, we have tested the effects of 10 M 5HT, a concentration that was shown to produce significant effects both in peripheral sensory organs (Rossi-Durand, 1993) and in the CNS (Pearlstein et al, 1998). When 5HT (10 M) was superfused on the ganglia (1 ml/min), two effects were observed on motor nerve activity: (1) the tonic background activity of MNs increased in both Dep and Lev MNs (see mean frequency traces in Fig.…”

Section: Ht Enhances Resistance Reflexmentioning

confidence: 99%

“…These two levels of a network have been shown to be controlled by neuromodulators in vertebrates and invertebrates (Hultborn and Kiehn, 1992;Katz, 1998;Sillar et al, 1998;Cantrell and Catterall, 2001;Nusbaum et al, 2001;Marder and Thirumalai, 2002). In crustacea, serotonin (5HT) was shown to modify synaptic transmission (Fischer and Florey, 1983;Delaney et al, 1991;Pearlstein et al, 1998;Wang and Zucker, 1998;Southard et al, 2000) and endogenous properties of neurons (Rossi-Durand, 1993;Alvarado-Alvarez et al, 2000;Nagayama, 2002). At the behavioral level 5HT can influence posture and walking (Teshiba et al, 2001;Tierney and Mangiamele, 2001), aggressiveness (Huber et al, 1997a,b), and social status in crayfish (Huber et al, 1997b(Huber et al, , 2001.…”

Section: Introductionmentioning

confidence: 99%

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

Bon-Jégo

Cattaert²,

Pearlstein³

2004

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.

“…In the last case serotonin, like AST, decreases the spike rate (Birmingham et al, 2003). In contrast, serotonin increases the static and dynamic response of crustacean chordotonal afferents (el Manira et al, 1991;Rossi-Durand, 1993) in a dosedependent manner and also increases the input resistance of leg motor neurons that receive input from chordotonal afferents (Le Bon-Jego et al, 2004). We repeated the CBCTO experimental protocol described above to test whether serotonin also modified the spike-timing precision.…”

Section: Cbcto Spike Rate and Jitter Increase In Serotoninmentioning

confidence: 99%

Neuromodulation of Spike-Timing Precision in Sensory Neurons

Billimoria

DiCaprio²,

Birmingham³

et al. 2006

The neuropeptide allatostatin decreases the spike rate in response to time-varying stretches of two different crustacean mechanoreceptors, the gastropyloric receptor 2 in the crab Cancer borealis and the coxobasal chordotonal organ (CBCTO) in the crab Carcinus maenas. In each system, the decrease in firing rate is accompanied by an increase in the timing precision of spikes triggered by discrete temporal features in the stimulus. This was quantified by calculating the standard deviation or "jitter" in the times of individual identified spikes elicited in response to repeated presentations of the stimulus. Conversely, serotonin increases the firing rate but decreases the timing precision of the CBCTO response. Intracellular recordings from the afferents of this receptor demonstrate that allatostatin increases the conductance of the neurons, consistent with its inhibitory action on spike rate, whereas serotonin decreases the overall membrane conductance. We conclude that spike-timing precision of mechanoreceptor afferents in response to dynamic stimulation can be altered by neuromodulators acting directly on the afferent neurons.