From tadpole to adult frog locomotion

Sillar, Keith T.; Simmers, John; Combes, Denis

doi:10.1016/j.conb.2023.102753

Cited by 9 publications

(3 citation statements)

References 45 publications

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“…Oscillatory networks, including central pattern generator (CPG) networks generating rhythmic patterns such as walking, breathing, and chewing are highly modulated to promote adaptation (1)(2)(3)(4)(5)(6)(7)(8)(9). CPG flexibility includes neuronal switching, where neuronal participation changes from one network to another, or to multiple networks, via neuromodulation of intrinsic and/or synaptic properties (10)(11)(12)(13)(14)(15)(16)(17).…”

Section: Introductionmentioning

confidence: 99%

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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Section: Introductionmentioning

confidence: 99%

Switching Neuron Contributions to Second Network Activity

Fahoum,

Blitz

2023

Preprint

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“…More complex behavioral interactions may also occur, such as nesting of the mouse crying rhythm nested within respiration, or dynamic changes in respiration during singing in mice, birds, or humans, or while playing wind instruments (Fortune et al, 2011;Hérent et al, 2023;Higashino et al, 2022;Okobi et al, 2019;Wei et al, 2022). Further, coordination can be altered by developmental, physiological, or environmental stimuli Clemens et al, 1998a;Moore et al, 2013;Saunders et al, 2004;Sillar et al, 2023;Stein and Harzsch, 2021). Although insights have been gained into internetwork coordination, its complexity and plasticity coupled, with often large, distributed networks make it difficult to fully determine how network coordination is controlled (Juvin et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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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“…More complex behavioral interactions may also occur, such as variations in respiration during crying, singing, or while playing wind instruments ( Fortune et al, 2011 ; Okobi et al, 2019 ; Higashino et al, 2022 ; Wei et al, 2022 ; Hérent et al, 2023 ). Further, coordination can be altered by developmental, physiological, or environmental stimuli ( Clemens et al, 1998a ; Saunders et al, 2004 ; Blitz and Nusbaum, 2008 ; Moore et al, 2013 ; Stein and Harzsch, 2021 ; Sillar et al, 2023 ). Although insights have been gained into internetwork coordination, its complexity and plasticity coupled with often large, distributed networks make it difficult to fully determine how network coordination is controlled ( Juvin et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Neuropeptide Modulation Enables Biphasic Internetwork Coordination via a Dual-Network Neuron

Gnanabharathi,

Fahoum,

Blitz

2024

eNeuro

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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 inter-network 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 neuropeptide modulatory state. Gly1-SIFamide 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 shorter cycles during gastric mill rhythm-timed LPG bursts, and longer cycles during IC, or IC plus LG gastric mill neuron bursts. Photoinactivation revealed that LPG is necessary to shorten pyloric cycle period, likely through its rectified electrical coupling to pyloric pacemaker neurons. Hyperpolarizing current injections demonstrated that although LG bursting enables IC bursts, only gastric mill rhythm bursts in IC are necessary to prolong the pyloric cycle period. Surprisingly, LPG photoinactivation also eliminated prolonged pyloric cycles, without changing IC firing frequency or gastric mill burst duration, suggesting that pyloric cycles are prolonged via IC synaptic inhibition of LPG, which indirectly slows the pyloric pacemakers via electrical coupling. Thus, the same dual-network neuron directly conveys excitation from its endogenous bursting and indirectly funnels synaptic inhibition to enable one network to alternately decrease and increase the cycle period 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 shortens fast network cycles during its slow, intrinsically generated bursts, likely via electrical coupling to fast network pacemakers, despite rectification favoring the opposite direction. Additionally, the fast network is indirectly prolonged during another slow-network phase, via chemical synaptic inhibition that is likely funneled through the same electrical synapse. Thus, a dual-network neuron 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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From tadpole to adult frog locomotion

Cited by 9 publications

References 45 publications

Switching Neuron Contributions to Second Network Activity

Switching Neuron Contributions to Second Network Activity

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

Neuropeptide Modulation Enables Biphasic Internetwork Coordination via a Dual-Network Neuron

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