Neuronal Switching Between Single- and Dual-Network Activity via Modulation of Intrinsic Membrane Properties

Fahoum, Savanna-Rae H.; Blitz, Dawn M.

doi:10.1101/2021.02.05.429848

Cited by 4 publications

(63 citation statements)

References 103 publications

(204 reference statements)

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“…This network plasticity results in multiple versions of rhythmic locomotor, respiratory and chewing behaviors, and different oscillatory patterns contributing to sleep, memory formation, and other cognitive processing (Barlow 2009; Cropper et al 2017; Dickinson 1995; Rangel et al 2016; Roopun et al 2008; Stickford and Stickford 2014). Network flexibility extends to neuronal switching, in which neurons change their participation between networks, including switching between single- and dual-frequency oscillations (Fahoum and Blitz 2021; Hooper and Moulins 1990; Meyrand et al 1994; Steriade et al 1993; Tryba et al 2008; Weimann et al 1991).…”

Section: Introductionmentioning

confidence: 99%

“…The sensitivity of the C. borealis STG networks to many neuromodulators correlates with a varied diet of this species (Dickinson et al 2008; Donahue et al 2009; Stehlik 1993). Particularly relevant to this study, flexibility of STNS network output in multiple crab and lobster species includes neuronal switching between pyloric, gastric mill, and swallowing networks (Blitz et al 2019; Fahoum and Blitz 2021; Hooper and Moulins 1990; Meyrand et al 1994).…”

Section: Introductionmentioning

confidence: 99%

“…A modulatory projection neuron, modulatory commissural neuron 5 (MCN5), uses the neuropeptide Gly 1 -SIFamide to elicit a particular gastric mill motor pattern, including interactions between the pyloric and gastric mill networks that differ from those during activation of other modulatory inputs (Blitz et al 2019; Fahoum and Blitz 2021). As part of its actions, MCN5 stimulation, or bath-applied Gly 1 -SIFamide, switches the lateral posterior gastric (LPG) neuron from solely being active with the pyloric rhythm, to dual- frequency bursting in time with the pyloric and gastric mill rhythms (Blitz et al 2019; Fahoum and Blitz 2021). In C. borealis , LPG typically generates fast (∼1 Hz) bursts due to electrical coupling with the other pyloric pacemaker ensemble neurons (Blitz et al 2019; Fahoum and Blitz 2021; Shruti et al 2014).…”

Section: Introductionmentioning

confidence: 99%

“…As part of its actions, MCN5 stimulation, or bath-applied Gly 1 -SIFamide, switches the lateral posterior gastric (LPG) neuron from solely being active with the pyloric rhythm, to dual- frequency bursting in time with the pyloric and gastric mill rhythms (Blitz et al 2019; Fahoum and Blitz 2021). In C. borealis , LPG typically generates fast (∼1 Hz) bursts due to electrical coupling with the other pyloric pacemaker ensemble neurons (Blitz et al 2019; Fahoum and Blitz 2021; Shruti et al 2014). However, in the MCN5/Gly 1 -SIFamide modulatory state, LPG generates pyloric-timed bursts, due to continued electrical coupling to pyloric pacemaker neurons, plus slower, gastric mill-timed bursts that are generated due to Gly 1 -SIFamide modulation of LPG intrinsic properties (Blitz et al 2019; Fahoum and Blitz 2021).…”

Section: Introductionmentioning

confidence: 99%

“…In C. borealis , LPG typically generates fast (∼1 Hz) bursts due to electrical coupling with the other pyloric pacemaker ensemble neurons (Blitz et al 2019; Fahoum and Blitz 2021; Shruti et al 2014). However, in the MCN5/Gly 1 -SIFamide modulatory state, LPG generates pyloric-timed bursts, due to continued electrical coupling to pyloric pacemaker neurons, plus slower, gastric mill-timed bursts that are generated due to Gly 1 -SIFamide modulation of LPG intrinsic properties (Blitz et al 2019; Fahoum and Blitz 2021). The membrane properties underlying the switch from single to dual-network activity have not been determined (Fahoum and Blitz 2021).…”

Section: Introductionmentioning

confidence: 99%

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Multiple Intrinsic Membrane Properties are Modulated in a Switch from Single to Dual-Network Activity

Snyder

Blitz

2022

Preprint

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Neural network flexibility extends to changes in neuronal participation between networks. This neuronal switching can include neurons moving between single- and dual-network activity. We previously identified an example in which bursting at a second frequency occurs due to modulation of intrinsic membrane properties instead of synaptic recruitment into a second network. However, the intrinsic properties that are modulated were not determined. Here, we use small networks in the Jonah crab (Cancer borealis) stomatogastric nervous system (STNS) to examine modulation of intrinsic properties underlying neuropeptide- (Gly1-SIFamide) elicited neuronal switching. The LPG neuron switches from exclusive participation in the fast pyloric (~1 Hz) network, due to electrical coupling, to dual-network activity which includes periodic escapes from the fast rhythm via intrinsically-generated oscillations at the slower gastric mill network frequency (~0.1 Hz). We isolated LPG from both networks using pharmacology and hyperpolarizing current injection. Gly1-SIFamide increased LPG intrinsic excitability and rebound from inhibition, and decreased spike frequency adaptation, which can all contribute to intrinsic bursting. Using ion substitution and channel blockers, we found that a hyperpolarization-activated current, a persistent sodium current, and a calcium or calcium-related current(s) appear to be primary contributors to Gly1-SIFamide-elicited LPG intrinsic bursting. However, this intrinsic bursting was more sensitive to blocking currents when LPG received rhythmic electrical coupling input from the fast network than in the isolated condition. Overall, a switch from single- to dual-network activity can involve modulation of multiple intrinsic properties, while synaptic input from a second network can shape the contributions of these properties.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Multiple Intrinsic Membrane Properties are Modulated in a Switch from Single to Dual-Network Activity

Snyder

Blitz

2022

Preprint

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Switching Neuron Contributions to Second Network Activity

Fahoum,

Blitz

2023

Preprint

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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.

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

Gnanabharathi,

Fahoum,

Blitz

2024

Preprint

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Linked rhythmic behaviors, such as respiration/locomotion or swallowing/chewing often require coordination for proper function. Despite its prevalence, the cellular mechanisms controlling coordination of the underlying neural networks remain undetermined in most systems. We use the stomatogastric nervous system of the crabCancer borealisto investigate mechanisms of internetwork coordination, due to its small, well characterized feeding-related networks (gastric mill [chewing, ∼0.1 Hz]; pyloric [filtering food, ∼1 Hz]). Here, we investigate coordination between these networks during the Gly1-SIFamide (SIF) neuropeptide modulatory state. SIF activates a unique triphasic gastric mill rhythm in which the typically pyloric-only LPG neuron generates dual pyloric-plus gastric mill-timed oscillations. Additionally, the pyloric rhythm exhibits increased cycle frequency during gastric mill rhythm-timed LPG bursts, and decreased cycle frequency during IC, or IC plus LG gastric mill neuron bursts. Hyperpolarizing current injections and photoinactivation of network neurons demonstrate that gastric mill rhythm bursts in IC, but not LG, are responsible for decreasing the pyloric frequency, whereas LPG increases pyloric frequency through its rectified electrical coupling to pyloric pacemaker neurons. Surprisingly, LPG photoinactivation also eliminated slowing of the pyloric rhythm. IC firing frequency and gastric mill burst duration were not altered by LPG photoinactivation, suggesting that IC slows the pyloric rhythm primarily via synaptic inhibition of LPG, which then slows the pyloric pacemakers via electrical coupling. Thus, despite its rectification, an electrical synapse directly conveys endogenous bursting and indirectly funnels neurotransmitter-mediated inhibition to enable one network to alternately increase and decrease the frequency of a related network.Significance StatementRelated rhythmic behaviors frequently exhibit coordination, yet the cellular mechanisms coordinating the underlying neural networks are not determined in most systems. We investigated coordination between two small, well-characterized crustacean feeding-associated networks during a neuropeptide-elicited modulatory state. We find that a dual fast/slow network neuron directly increases fast network frequency during its slow, intrinsically generated bursts, via electrical coupling to fast network pacemakers, despite rectification favoring the opposite direction. Additionally, the fast network is indirectly slowed during another slow-network phase, via chemical synaptic inhibition funneled through the same electrical synapse. Thus, a rectifying electrical synapse alternately reinforces and diminishes neuropeptide actions, enabling distinct frequencies of a faster network across different phases of a related slower rhythm.

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Neuronal Switching Between Single- and Dual-Network Activity via Modulation of Intrinsic Membrane Properties

Cited by 4 publications

References 103 publications

Multiple Intrinsic Membrane Properties are Modulated in a Switch from Single to Dual-Network Activity

Multiple Intrinsic Membrane Properties are Modulated in a Switch from Single to Dual-Network Activity

Switching Neuron Contributions to Second Network Activity

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

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