TY - JOUR
T1 - Distinct mechanisms underlie electrical coupling resonance and its interaction with membrane potential resonance
AU - Li, Xinping
AU - Itani, Omar
AU - Bucher, Dirk M.
AU - Rotstein, Horacio G.
AU - Nadim, Farzan
N1 - Publisher Copyright:
Copyright © 2023 Li, Itani, Bucher, Rotstein and Nadim.
PY - 2023
Y1 - 2023
N2 - Neurons in oscillatory networks often exhibit membrane potential resonance, a peak impedance at a non-zero input frequency. In electrically coupled oscillatory networks, the coupling coefficient (the ratio of post- and prejunctional voltage responses) could also show resonance. Such coupling resonance may emerge from the interaction between the coupling current and resonance properties of the coupled neurons, but this relationship has not been clearly described. Additionally, it is unknown if the gap-junction mediated electrical coupling conductance may have frequency dependence. We examined these questions by recording a pair of electrically coupled neurons in the oscillatory pyloric network of the crab Cancer borealis. We performed dual current- and voltage-clamp recordings and quantified the frequency preference of the coupled neurons, the coupling coefficient, the electrical conductance, and the postjunctional neuronal response. We found that all components exhibit frequency selectivity, but with distinct preferred frequencies. Mathematical and computational analysis showed that membrane potential resonance of the postjunctional neuron was sufficient to give rise to resonance properties of the coupling coefficient, but not the coupling conductance. A distinct coupling conductance resonance frequency therefore emerges either from other circuit components or from the gating properties of the gap junctions. Finally, to explore the functional effect of the resonance of the coupling conductance, we examined its role in synchronizing neuronal the activities of electrically coupled bursting model neurons. Together, our findings elucidate factors that produce electrical coupling resonance and the function of this resonance in oscillatory networks.
AB - Neurons in oscillatory networks often exhibit membrane potential resonance, a peak impedance at a non-zero input frequency. In electrically coupled oscillatory networks, the coupling coefficient (the ratio of post- and prejunctional voltage responses) could also show resonance. Such coupling resonance may emerge from the interaction between the coupling current and resonance properties of the coupled neurons, but this relationship has not been clearly described. Additionally, it is unknown if the gap-junction mediated electrical coupling conductance may have frequency dependence. We examined these questions by recording a pair of electrically coupled neurons in the oscillatory pyloric network of the crab Cancer borealis. We performed dual current- and voltage-clamp recordings and quantified the frequency preference of the coupled neurons, the coupling coefficient, the electrical conductance, and the postjunctional neuronal response. We found that all components exhibit frequency selectivity, but with distinct preferred frequencies. Mathematical and computational analysis showed that membrane potential resonance of the postjunctional neuron was sufficient to give rise to resonance properties of the coupling coefficient, but not the coupling conductance. A distinct coupling conductance resonance frequency therefore emerges either from other circuit components or from the gating properties of the gap junctions. Finally, to explore the functional effect of the resonance of the coupling conductance, we examined its role in synchronizing neuronal the activities of electrically coupled bursting model neurons. Together, our findings elucidate factors that produce electrical coupling resonance and the function of this resonance in oscillatory networks.
KW - central pattern generator
KW - gap junctions
KW - oscillation
KW - resonance
KW - stomatogastric
UR - http://www.scopus.com/inward/record.url?scp=85182243877&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85182243877&partnerID=8YFLogxK
U2 - 10.3389/fsysb.2023.1122433
DO - 10.3389/fsysb.2023.1122433
M3 - Article
AN - SCOPUS:85182243877
SN - 2674-0702
VL - 3
JO - Frontiers in Systems Biology
JF - Frontiers in Systems Biology
M1 - 1122433
ER -