Nitric oxide-mediated intersegmental modulation of cycle frequency in the crayfish swimmeret system

Abstract

Crayfish swimmerets are paired appendages located on the ventral side of each abdominal segment that show rhythmic beating during forward swimming produced by central pattern generators in most abdominal segments. For animals with multiple body segments and limbs, intersegmental coordination of central pattern generators in each segment is crucial for the production of effective movements. Here we develop a novel pharmacological approach to analyse intersegmental modulation of swimmeret rhythm by selectively elevating nitric oxide levels and reducing them with pharmacological agents, in specific ganglia. Bath application of L-arginine, the substrate NO synthesis, increased the cyclical spike responses of the power-stroke motor neurons. By contrast the NOS inhibitor, L-NAME decreased them. To determine the role of the different local centres in producing and controlling the swimmeret rhythm, these two drugs were applied locally to two separate ganglia following bath application of carbachol. Results revealed that there was both ascending and descending intersegmental modulation of cycle frequency of the swimmeret rhythm in the abdominal ganglia and that synchrony of cyclical activity between segments of segments was maintained. We also found that there were gradients in the strength effectiveness in modulation, that ascending modulation of the swimmeret rhythm was stronger than descending modulation.

Nitric oxide mediates activity-dependent change to synaptic excitation during a critical period in Drosophila

“…Our results show that NO-signaling mediates specification of both neuronal excitable and synaptic transmission properties, in at least two layers of the locomotor network. This is in line with increasing evidence for nitrergic modulation of rhythmic motor activity produced by central pattern generators in both vertebrates 25 – 27 and invertebrates 28 , 29 . It is conceivable that change to synaptic transmission results from structural change to synaptic architecture in either, or both, pre and postsynaptic compartments.…”

Novel Insights on Nitric Oxide Synthase and NO Signaling in Ascidian Metamorphosis

“…The correlation between NO and the control of rhythmic motor activity and swimming speed induced by CPG is further supported by the presence of NOS and NO in the tail sensory neurons. A role for NO in the control of mechanosensory processing has been well-described in both invertebrates and vertebrates [ 85 , 88 , 89 , 90 , 91 ]. It was already evidenced in the invertebrate locust, where it was suggested that NO acted as a modulator of the input from the sensory neurons and the output of motor neurons [ 92 , 93 ].…”

A common role for astrocytes in rhythmic behaviours?

“…Spinal locomotor networks are subject to considerable modulation from various neural sources, both within the spinal cord and from descending inputs. Numerous different neurotransmitters including monoamines (Han et al, 2007;Kiehn et al, 1999;Schmidt & Jordan, 2000;Sharples et al, 2015), acetylcholine (Jordan et al, 2014;Nascimento et al, 2019Nascimento et al, , 2020, nitric oxide (Foster et al, 2014;Yoshida et al, 2018) and adenosine (Acton & Miles, 2017;Brown & Dale, 2000) have been shown to modulate locomotor output in terms of the frequency of motor bursts, their duration and their amplitude. Moreover, many of these neuromodulators may work together in order to elicit different effects -termed metamodulation (Acton & Miles, 2017;McLean & Sillar, 2004;Sharples et al, 2015).…”