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

Abstract

SUMMARY The biological mechanisms of behavioral selection, as it relates to locomotion, are far from understood, even in relatively simple invertebrate animals. In the medicinal leech, Hirudo medicinalis, the decision to swim is distributed across populations of swim-activating and swim-inactivating neurons descending from the subesophageal ganglion of the compound cephalic ganglion, i.e. the brain. In the present study, we demonstrate that the serotonergic LL and Retzius cells in the brain are excited by swim-initiating stimuli and during spontaneous swim episodes. This activity likely influences or resets the neuromodulatory state of neural circuits involved in the activation or subsequent termination of locomotion. When serotonin (5-HT) was perfused over the brain, multi-unit recordings from descending brain neurons revealed rapid and substantial alterations. Subsequent intracellular recordings from identified command-like brain interneurons demonstrated that 5-HT, especially in combination with octopamine, inhibited swim-triggering neuron Tr1, as well as swim-inactivating neurons Tr2 and SIN1. Although 5-HT inhibited elements of the swim-inactivation pathway, rather than promoting them, the indirect and net effect of the amine was a reliable and sustained reduction in the firing of the segmental swim-gating neuron 204. This modulation caused cell 204 to relinquish its excitatory drive to the swim central pattern generator. The activation pattern of serotonergic brain neurons that we observed during swimming and the 5-HT-immunoreactive staining pattern obtained, suggest that within the head brain 5-HT secretion is massive. Over time, 5-HT secretion may provide a homeostatic feedback mechanism to limit swimming activity at the level of the head brain.

Statistical characterization of social interactions and collective behavior in medicinal leeches

“…4, B and C). The change in the modal duration suggests that other modulatory effects could be present in different regions: for example, it is known that the head brain contributes not only to swimming initiation but also to the quality (duration and rhythmicity) of these episodes (Crisp and Mesce 2006).…”

Detection and selective avoidance of near ultraviolet radiation by an aquatic annelid: the medicinal leech

“…It has been well established that satiety strongly influences sensory responses (Gaudry and Kristan, 2009) and the probability of evoking certain behaviors, such as swimming or crawling (Gaudry and Kristan, 2010;Misell et al, 1998). Many of the interactions influencing motivation, behavioral choice and responses to stimuli are regulated by amines (Crisp and Mesce, 2006;Esch et al, 2002;Nusbaum, 1982-1983;Puhl and Mesce, 2008) and these transmitter systems strongly interact with feeding behavior, swimming and crawling (Brodfuehrer and Friesen, 1984;Lent and Dickinson, 1984;Willard, 1981). Since unfed individuals were expected to be less averse to visible light than fed (consistent with the results for visible light in these studies as well; see Tables 1, 2), I expected that unfed individuals might not exhibit as strong a negative phototaxis to UVR.…”

Dopamine Activates the Motor Pattern for Crawling in the Medicinal Leech

“…Swimming has been thoroughly described at the level of its patterngenerating neural networks (Brodfuehrer and Thorogood, 2001;Brodfuehrer et al, 1995a), gating cells (Kristan and Weeks, 1983), descending command-like cells (Brodfuehrer and Friesen, 1986;Brodfuehrer et al, 1995b;O'Gara and Friesen, 1995;Esch et al, 2002), and modulation by serotonin Crisp and Mesce, 2006). Insights into the neuronal bases of both these locomotor patterns can now be advanced by comparing their organization and regulation.…”