article · 15/09/2021
Trans-inhibition of axon terminals underlies competition in the habenulo-interpeduncular pathway
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Résumé
Survival of animals is dependent on the correct selection of an appropriate behavioral response to competing external stimuli. Theoretical models have been proposed and underlying mechanisms are emerging to explain how one circuit is selected among competing neural circuits. The evolutionarily conserved forebrain to midbrain habenulo-interpeduncular nucleus (Hb-IPN) pathway consists of cholinergic and non-cholinergic neurons, which mediate different aversive behaviors. Simultaneous calcium imaging of neuronal cell bodies and of the population dynamics of their axon terminals reveals that signals in the cell bodies are not reflective of terminal activity. We find that axon terminals of cholinergic and non-cholinergic habenular neurons exhibit stereotypic patterns of spontaneous activity that are negatively correlated and localize to discrete subregions of the target IPN. Patch-clamp recordings show that calcium bursts in cholinergic terminals at the ventral IPN trigger excitatory currents in IPN neurons, which precede inhibition of non-cholinergic terminals at the adjacent dorsal IPN. Inhibition is mediated through presynaptic GABAB receptors activated in non-cholinergic habenular neurons upon GABA release from the target IPN. Together, the results reveal a hardwired mode of competition at the terminals of two excitatory neuronal populations, providing a physiological framework to explore the relationship between different aversive responses.
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Zaupa, M., Alavi Naini, S.-M., Younes, M.-A., Bullier, E., Duboué, E.-R., Le Corronc, H., Soula, H., Wolf, S., Candelier, R., Legendre, P., Halpern, M.-E., Mangin, J.-M., & Hong, E. (2021). Trans-inhibition of axon terminals underlies competition in the habenulo-interpeduncular pathway. Current Biology. https://doi.org/10.1016/j.cub.2021.08.051@article{Zaupa2021_336,
author = {Zaupa, Margherita and Alavi Naini, Seyedeh Maryam and Younes, Maroun Abi and Bullier, Erika and Duboué, Erik R. and Le Corronc, Hervé and Soula, Hédi and Wolf, Sebastien and Candelier, Raphaël and Legendre, Pascal and Halpern, Marnie E. and Mangin, Jean-Marie and Hong, Elim},
year = {2021},
month = {9},
title = {Trans-inhibition of axon terminals underlies competition in the habenulo-interpeduncular pathway},
journal = {Current Biology},
abstract = {Survival of animals is dependent on the correct selection of an appropriate behavioral response to competing external stimuli. Theoretical models have been proposed and underlying mechanisms are emerging to explain how one circuit is selected among competing neural circuits. The evolutionarily conserved forebrain to midbrain habenulo-interpeduncular nucleus (Hb-IPN) pathway consists of cholinergic and non-cholinergic neurons, which mediate different aversive behaviors. Simultaneous calcium imaging of neuronal cell bodies and of the population dynamics of their axon terminals reveals that signals in the cell bodies are not reflective of terminal activity. We find that axon terminals of cholinergic and non-cholinergic habenular neurons exhibit stereotypic patterns of spontaneous activity that are negatively correlated and localize to discrete subregions of the target IPN. Patch-clamp recordings show that calcium bursts in cholinergic terminals at the ventral IPN trigger excitatory currents in IPN neurons, which precede inhibition of non-cholinergic terminals at the adjacent dorsal IPN. Inhibition is mediated through presynaptic GABAB receptors activated in non-cholinergic habenular neurons upon GABA release from the target IPN. Together, the results reveal a hardwired mode of competition at the terminals of two excitatory neuronal populations, providing a physiological framework to explore the relationship between different aversive responses.},
url = {https://www.sciencedirect.com/science/article/pii/S0960982221011878},
doi = {10.1016/j.cub.2021.08.051},
issn = {0960-9822},
}TY - JOUR
AU - Zaupa, Margherita
AU - Alavi Naini, Seyedeh Maryam
AU - Younes, Maroun Abi
AU - Bullier, Erika
AU - Duboué, Erik R.
AU - Le Corronc, Hervé
AU - Soula, Hédi
AU - Wolf, Sebastien
AU - Candelier, Raphaël
AU - Legendre, Pascal
AU - Halpern, Marnie E.
AU - Mangin, Jean-Marie
AU - Hong, Elim
PY - 2021
DA - 2021/09/15
TI - Trans-inhibition of axon terminals underlies competition in the habenulo-interpeduncular pathway
JO - Current Biology
SN - 0960-9822
AB - Survival of animals is dependent on the correct selection of an appropriate behavioral response to competing external stimuli. Theoretical models have been proposed and underlying mechanisms are emerging to explain how one circuit is selected among competing neural circuits. The evolutionarily conserved forebrain to midbrain habenulo-interpeduncular nucleus (Hb-IPN) pathway consists of cholinergic and non-cholinergic neurons, which mediate different aversive behaviors. Simultaneous calcium imaging of neuronal cell bodies and of the population dynamics of their axon terminals reveals that signals in the cell bodies are not reflective of terminal activity. We find that axon terminals of cholinergic and non-cholinergic habenular neurons exhibit stereotypic patterns of spontaneous activity that are negatively correlated and localize to discrete subregions of the target IPN. Patch-clamp recordings show that calcium bursts in cholinergic terminals at the ventral IPN trigger excitatory currents in IPN neurons, which precede inhibition of non-cholinergic terminals at the adjacent dorsal IPN. Inhibition is mediated through presynaptic GABAB receptors activated in non-cholinergic habenular neurons upon GABA release from the target IPN. Together, the results reveal a hardwired mode of competition at the terminals of two excitatory neuronal populations, providing a physiological framework to explore the relationship between different aversive responses.
DO - 10.1016/j.cub.2021.08.051
UR - https://www.sciencedirect.com/science/article/pii/S0960982221011878
ER -