Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia

The expression of motivated behaviors depends on both external and internally-arising neural stimuli, yet the intrinsic releasing mechanisms for such variably occurring behaviors remain elusive. In isolated nervous system preparations of Aplysia, we have found that irregularly expressed cycles of motor output underlying food-seeking behavior arise from regular membrane potential oscillations of varying magnitude in an identified pair of interneurons (B63) in the bilateral buccal ganglia. This rhythmic signal, which is specific to the B63 cells, is generated by organelle-derived intracellular calcium fluxes that activate voltage-independent plasma membrane channels. The resulting voltage oscillation spreads throughout a subset of gap junction-coupled buccal network neurons and by triggering plateau potential-mediated bursts in B63, can initiate motor output driving food-seeking action. Thus, an atypical neuronal pacemaker mechanism, based on rhythmic intracellular calcium store release and intercellular propagation, can act as an autonomous intrinsic releaser for the occurrence of a motivated behavior.

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Organelle calcium-derived voltage oscillations in pacemaker neurons drive food-seeking behavior in Aplysia

10.1101/2021.03.30.437701 ◽

2021 ◽

Author(s):

Alexis Bédécarrats ◽

Laura Puygrenier ◽

John Castro O'Byrne ◽

Quentin Lade ◽

John Simmers ◽

...

Keyword(s):

Intracellular Calcium ◽

Motor Output ◽

Potential Oscillations ◽

Intracellular Calcium Store ◽

Voltage Oscillation ◽

Motivated Behavior ◽

Seeking Behavior ◽

Food Seeking ◽

Motivated Behaviors ◽

Membrane Potential Oscillations

The expression of motivated behaviors depends on both external and internally-arising neural stimuli, yet the intrinsic releasing mechanisms for such variably occurring behaviors remain elusive. In isolated nervous system preparations of Aplysia, we have found that irregularly expressed cycles of motor output underlying food-seeking behavior arise from regular membrane potential oscillations of varying magnitude in an identified pair of interneurons (B63) in the bilateral buccal ganglia. This rhythmic signal, which is endogenous and specific to the B63 cells, is generated by organelle-derived intracellular calcium fluxes that activate voltage-independent plasma membrane channels. The resulting voltage oscillation spreads throughout a subset of gap junction-coupled buccal network neurons and by triggering plateau potential-mediated bursts in B63, can initiate motor output driving food-seeking action. Thus, an atypical neuronal pacemaker mechanism, based on rhythmic intracellular calcium store release and intercellular propagation, can act as an autonomous intrinsic releaser for the occurrence of a motivated behavior.

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Faculty Opinions recommendation of Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.740397363.793589755 ◽

2021 ◽

Author(s):

Björn Brembs

Keyword(s):

Motor Program ◽

Pacemaker Neurons ◽

Seeking Behavior ◽

Food Seeking

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Release of a single neurotransmitter from an identified interneuron coherently affects motor output on multiple time scales

Journal of Neurophysiology ◽

10.1152/jn.01079.2012 ◽

2013 ◽

Vol 109 (9) ◽

pp. 2327-2334 ◽

Cited By ~ 4

Author(s):

Andrew M. Dacks ◽

Klaudiusz R. Weiss

Keyword(s):

Time Scales ◽

Motor Program ◽

Gaba Release ◽

Motor Output ◽

Multiple Time Scales ◽

Multiple Time ◽

Intrinsic Properties ◽

Buccal Ganglion ◽

Motor Programs ◽

Pattern Characteristic

Neurotransmitters can have diverse effects that occur over multiple time scales often making the consequences of neurotransmission difficult to predict. To explore the consequences of this diversity, we used the buccal ganglion of Aplysia to examine the effects of GABA release by a single interneuron, B40, on the intrinsic properties and motor output of the radula closure neuron B8. B40 induces a picrotoxin-sensitive fast IPSP lasting milliseconds in B8 and a slow EPSP lasting seconds. We found that the excitatory effects of this slow EPSP are also mediated by GABA. Together, these two GABAergic actions structure B8 firing in a pattern characteristic of ingestive programs. Furthermore, we found that repeated B40 stimulation induces a persistent increase in B8 excitability that was occluded in the presence of the GABA B receptor agonist baclofen, suggesting that GABA affects B8 excitability over multiple time scales. The phasing of B8 activity during the feeding motor programs determines the nature of the behavior elicited during that motor program. The persistent increase in B8 excitability induced by B40 biased the activity of B8 during feeding motor programs causing the motor programs to become more ingestive in nature. Thus, a single transmitter released from a single interneuron can have consequences for motor output that are expressed over multiple time scales. Importantly, despite the differences in their signs and temporal characteristics, the three actions of B40 are coherent in that they promote B8 firing patterns that are characteristic of ingestive motor outputs.

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The sigma-1 receptor as key common factor in cocaine and food-seeking behaviors

Journal of Molecular Endocrinology ◽

10.1530/jme-19-0138 ◽

2019 ◽

Vol 63 (4) ◽

pp. R81-R92 ◽

Cited By ~ 1

Author(s):

David Aguinaga ◽

Mireia Casanovas ◽

Rafael Rivas-Santisteban ◽

Irene Reyes-Resina ◽

Gemma Navarro ◽

...

Keyword(s):

Eating Disorders ◽

Drugs Of Abuse ◽

Common Factor ◽

G Protein Coupled Receptors ◽

Sigma 1 Receptor ◽

New Findings ◽

Sigma 1 ◽

Seeking Behavior ◽

Food Seeking ◽

G Protein Coupled

Addiction and eating disorders involve brain reward circuits. Binge eating predisposes to addictive behavior, while the cessation of exposure to drugs of abuse leads to reward activities, including intake of tasty foods. Cocaine use is associated with a decrease in food intake, with reversal after drug use is discontinued. Exciting new findings show that receptors for the ‘hunger’ hormone, ghrelin, directly interact with the sigma-1 receptor (σ1R), which is a target of cocaine. σ1Rs are key players in regulating dopaminergic neurotransmission and ghrelin-mediated actions. This review focuses on the σ1 receptor as a general neuroendocrine regulator by directly interacting with neuronal G-protein-coupled receptors. This review also covers the early mechanisms by which cocaine binding to σ1 blocks the food-seeking behavior triggered by ghrelin. Those findings appear as fundamental to understand common mechanisms in drug addiction and eating disorders.

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Cannabinoid Cb1 Receptor Antagonists/Inverse Agonists and Food-Seeking Behavior

Handbook of Behavior, Food and Nutrition ◽

10.1007/978-0-387-92271-3_29 ◽

2011 ◽

pp. 441-456

Author(s):

John D. Salamone ◽

Kelly Sink ◽

Kristen N. Segovia ◽

Patrick A. Randall ◽

Peter J. McLaughlin ◽

...

Keyword(s):

Cb1 Receptor ◽

Cannabinoid Cb1 Receptor ◽

Receptor Antagonists ◽

Inverse Agonists ◽

Seeking Behavior ◽

Food Seeking ◽

Cb1 Receptor Antagonists

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Changes in activity rates in the cherry shrimp Neocaridina davidi Bouvier, 1904 (Decapoda: Caridea: Atyidae) in response to concentrations of neuropeptides and glucose

Journal of Crustacean Biology ◽

10.1093/jcbiol/ruz059 ◽

2019 ◽

Vol 39 (6) ◽

pp. 689-694

Author(s):

Joseph S Stout ◽

Carla L Granda ◽

Molly L Mancuso

Keyword(s):

Food Pellet ◽

Inhibitory Effect ◽

Dopaminergic Drugs ◽

Behavioral Studies ◽

Seeking Behavior ◽

Food Seeking ◽

And Behavior ◽

Rats And Mice ◽

Reduced Activity ◽

Over Time

Abstract Although behavioral studies of whole animals are usually undertaken on rats and mice, studies in crustaceans offer an alternative group that provides new evolutionary insights into the relationship between physiology and behavior. In the cherry shrimp Neocaridina davidi (Bouvier, 1904), food-seeking movement increases in response to glutamate (MSG), decreases when exposed to dopamine, and increases when exposed to glucose. Activity of shrimp individuals was observed in 4l tanks over twenty minutes after individuals were exposed to treatments applied directly into the water. Glutamate-stimulated seeking behavior was statistically similar to seeking behavior after exposure to food pellet filtrate. Glucose also stimulated seeking behavior, but with a reduction over time, whereas MSG-stimulated seeking behavior increased over time. Insulin reduced activity but showed no effect when paired with glucose, whereas dopamine increased activity when paired with glucose. This was contrary to the reduced activity observed when dopamine was paired with MSG. The decrease in activity after exposure to dopamine also contrasts with vertebrate (rat) models where dopaminergic drugs such as caffeine and cocaine are stimulants. The stimulatory effect of dopamine paired with glucose was unexpected given its inhibitory effect on its own or when paired with MSG. This crustacean-based model aims to give new insights regarding the role of inhibitory and stimulatory neurotransmitters on the behavior of whole crustacean individuals. These mechanisms show different results than predicted by vertebrate models, implying either differences in underlying physiology, problems with the vertebrate models, or both.

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