Switching Neuron Contributions to Second Network Activity

Abstract

Network flexibility is important for adaptable behaviors. This includes neuronal switching, where neurons alter their network participation, including changing from single-to dual-network activity. Understanding the implications of neuronal switching requires determining how a switching neuron interacts with each of its networks. Here, we tested 1) whether “home” and second networks, operating via divergent rhythm generation mechanisms, regulate a switching neuron, and 2) if a switching neuron, recruited via modulation of intrinsic properties, contributes to rhythm or pattern generation in a new network. Small, well-characterized feeding-related networks (pyloric, ∼1 Hz; gastric mill, ∼0.1 Hz) and identified modulatory inputs make the isolated crab (Cancer borealis) stomatogastric nervous system (STNS) a useful model to study neuronal switching. In particular, the neuropeptide Gly1-SIFamide switches the lateral posterior gastric (LPG) neuron (2 copies) from pyloric-only to dual-frequency pyloric/gastric mill (fast/slow) activity via modulation of LPG intrinsic properties. Using current injections to manipulate neuronal activity, we found that gastric mill, but not pyloric, network neurons regulated the intrinsically generated LPG slow bursting. Conversely, selective elimination of LPG from both networks using photoinactivation revealed that LPG regulated gastric mill neuron firing frequencies but was not necessary for gastric mill rhythm generation or coordination. However, LPG alone was sufficient to produce a distinct pattern of network coordination. Thus, modulated intrinsic properties underlying dual-network participation may constrain which networks can regulate switching neuron activity. Further, recruitment via intrinsic properties may occur in modulatory states where it is important for the switching neuron to actively contribute to network output.New and NoteworthyWe used small, well-characterized networks to investigate interactions between rhythmic networks and neurons that switch their network participation. For a neuron switching into dual-network activity, only the second network regulated its activity in that network. Additionally, the switching neuron was sufficient but not necessary to coordinate second network neurons, and regulated their activity levels. Thus, regulation of switching neurons may be selective, and a switching neuron is not necessarily simply a follower in additional networks.

Neuropeptide Modulation Enables Biphasic Inter-network Coordination via a Dual-Network Neuron

“…8). In fact, we recently determined that Gly 1 -SIFamide enhances a typically ineffective IC to LPG graded glutamatergic synapse, enabling gastric mill IC bursts to regulate LPG gastric mill-timed activity (Fahoum and Blitz, 2023). The current study indicates that the modulated IC to LPG synapse also indirectly regulates the pyloric cycle period via LPG's electrical coupling to AB/PD.…”

“…However, this inhibition appears to act primarily via IC chemical synaptic inhibition of LPG (thick pink stick/ball), with a possible weak contribution via chemical inhibition of the AB and/or PD neuron (thin pink line/ball). The IC to LPG inhibitory synapse is strengthened during Gly 1 -SIFamide modulation (compare thin line/ball in saline to thick line/ball in Gly 1 -SIFamide; Fahoum and Blitz, 2023).…”

“…An in vitro STNS preparation includes the stomatogastric ganglion (STG, ~30 neurons) containing well-characterized CPGs that control the gastric mill (food chewing) and pyloric (food filtering) rhythms, plus identified modulatory and sensory inputs (Fig. 1) (Blitz, 2023;Daur et al, 2016;Nusbaum and Beenhakker, 2002). The pacemaker-driven pyloric rhythm is constitutively active in vivo and in vitro (~1 s cycle period), whereas the slower (~10 s cycle period) network-driven gastric mill CPG requires activation by modulatory or sensory inputs (Blitz, 2023;Nusbaum and Beenhakker, 2002).…”

“…1) (Blitz, 2023;Daur et al, 2016;Nusbaum and Beenhakker, 2002). The pacemaker-driven pyloric rhythm is constitutively active in vivo and in vitro (~1 s cycle period), whereas the slower (~10 s cycle period) network-driven gastric mill CPG requires activation by modulatory or sensory inputs (Blitz, 2023;Nusbaum and Beenhakker, 2002). All pyloric and gastric mill neurons (1-5 neurons/type) and their transmitters are identified, and their connectivity is mapped under multiple modulatory conditions (Fig.…”

Neuropeptide Modulation of Bidirectional Internetwork Synapses

“…The STG contains ~30 neurons that are interconnected to form well-characterized CPG networks which drive the pyloric and gastric mill rhythms. The CoGs and OG contain modulatory projection neurons that project to the STG and activate and modulate the pyloric and gastric mill CPGs (Blitz, 2023). The pyloric pacemaker interneuron, anterior burster (AB), is electrically coupled to the pyloric dilator (PD, 2 copies) and lateral posterior gastric (LPG, 2 copies) motor neurons, and together they form the pacemaker group for the pyloric rhythm (Marder & Eisen, 1984;Shruti et al, 2014) (Fig.…”