Function follows form: how the structure of neurons determines cortical network activity

Draguhn, Andreas; Both, Martin

doi:10.1007/s00424-022-02776-7

Cited by 3 publications

(1 citation statement)

References 10 publications

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“…A recent study by Hodapp et.al. suggested that neurons can escape the burden of perisomatic inhibition by relocating the axon initial segment from the heavily inhibited soma to one of the basal dendrites 19,20 . While cells with a privileged dendrite possessing the axon can indeed bypass perisomatic inhibition, making one dendrite privileged makes the rest of dendritic tree obsolete.…”

Section: Introductionmentioning

confidence: 99%

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Lebedeva,

Jappy,

Nasretdinov

et al. 2023

Preprint

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For over half a century, it has been postulated that the internal excitatory circuit in the hippocampus consists of three relay stations. Excitation arrives from the entorhinal cortex to the DG granule cells, is transmitted through the mossy fibers to CA3 pyramidal cells, and is then transmitted through Schaffer collaterals to CA1 pyramidal neurons. In all three structures (DG, CA3 and CA1), the activity of the excitatory neurons involved in the synaptic transmission of excitation are under the control of inhibitory basket neurons that are recruited into network activity via feed-forward and feed-back excitation. However, in the late 90s “stratum radiatum giant cells” were described as a novel type of neuron with the anatomical features of excitatory cells. Since then, the role of these cells in the hippocampal circuitry has not been well understood. Here, using optogenetic and electrophysiological techniques we characterized the functional location of these neurons within the hippocampal network. We show that: (i) the main excitatory drive to giant excitatory neurons in stratum radiatum (ExNR) comes via Schaffer collaterals; (ii) within the CA1 field, ExNRare not directly connected with local pyramidal cells, but provide massive and efficient excitatory input to parvalbumin positive (PV+) interneurons; (iii) ExNRare reciprocally innervated by bistratified cells, but not inhibited by backet interneurons; (iv) the efficiency of ExNRexcitation to PV+ interneurons is sufficient for a single ExNRaction potential to trigger massive inhibition of downstream CA1 pyramidal cells. Taken together, our data shows that ExNRconstitute an alternative pathway of excitation for CA1 interneurons that avoids the burden of perisomatic inhibition.

show abstract

Section: Introductionmentioning

confidence: 99%

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Lebedeva,

Jappy,

Nasretdinov

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Lebedeva,

Jappy,

Nasretdinov

et al. 2024

Preprint

View full text Add to dashboard Cite

For over half a century, it has been postulated that the internal excitatory circuit in the hippocampus consists of three relay stations. Excitation arrives from the entorhinal cortex to the DG granule cells, is transmitted through the mossy fibers to CA3 pyramidal cells, and is then transmitted through Schaffer collaterals to CA1 pyramidal neurons. In all three structures (DG, CA3 and CA1), the activity of the excitatory neurons involved in the synaptic transmission of excitation are under the control of inhibitory basket neurons that are recruited into network activity via feed-forward and feed-back excitation. However, in the late 90s “stratum radiatum giant cells” were described as a novel type of neuron with the anatomical features of excitatory cells. Since then, the role of these cells in the hippocampal circuitry has not been well understood. Here, using optogenetic and electrophysiological techniques we characterized the functional location of these neurons within the hippocampal network. We show that: (i) the main excitatory drive to giant excitatory neurons in stratum radiatum (ExN R ) comes via Schaffer collaterals; (ii) within the CA1 field, ExN R are not directly connected with local pyramidal cells, but provide massive and efficient excitatory input to parvalbumin positive (PV+) interneurons; (iii) ExN R are reciprocally innervated by bistratified cells, but not inhibited by backet interneurons; (iv) the efficiency of ExN R excitation to PV+ interneurons is sufficient for a single ExN R action potential to trigger massive inhibition of downstream CA1 pyramidal cells. Taken together, our data shows that ExN R constitute an alternative pathway of excitation for CA1 interneurons that avoids the burden of perisomatic inhibition.

show abstract

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Lebedeva,

Jappy,

Nasretdinov

et al. 2024

Preprint

View full text Add to dashboard Cite

For over half a century, it has been postulated that the internal excitatory circuit in the hippocampus consists of three relay stations. Excitation arrives from the entorhinal cortex to the DG granule cells, is transmitted through the mossy fibers to CA3 pyramidal cells, and is then transmitted through Schaffer collaterals to CA1 pyramidal neurons. In all three structures (DG, CA3 and CA1), the activity of the excitatory neurons involved in the synaptic transmission of excitation are under the control of inhibitory basket neurons that are recruited into network activity via feed-forward and feed-back excitation. However, in the late 90s “stratum radiatum giant cells” were described as a novel type of neuron with the anatomical features of excitatory cells. Since then, the role of these cells in the hippocampal circuitry has not been well understood. Here, using optogenetic and electrophysiological techniques we characterized the functional location of these neurons within the hippocampal network. We show that: (i) the main excitatory drive to giant excitatory neurons in stratum radiatum (ExN R ) comes via Schaffer collaterals; (ii) within the CA1 field, ExN R are not directly connected with local pyramidal cells, but provide massive and efficient excitatory input to parvalbumin positive (PV+) interneurons; (iii) ExN R are reciprocally innervated by bistratified cells, but not inhibited by backet interneurons; (iv) the efficiency of ExN R excitation to PV+ interneurons is sufficient for a single ExN R action potential to trigger massive inhibition of downstream CA1 pyramidal cells. Taken together, our data shows that ExN R constitute an alternative pathway of excitation for CA1 interneurons that avoids the burden of perisomatic inhibition.

show abstract

Function follows form: how the structure of neurons determines cortical network activity

Cited by 3 publications

References 10 publications

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

Excitatory neurons in stratum radiatum provide an alternative pathway for excitation flow that escapes perisomatic inhibition

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