Cortical interneurons: fit for function and fit to function? Evidence from development and evolution

dc.contributor.authorKeijser, Joram
dc.contributor.authorSprekeler, Henning
dc.date.accessioned2023-06-19T14:51:21Z
dc.date.available2023-06-19T14:51:21Z
dc.date.issued2023-05-04
dc.date.updated2023-06-15T12:22:36Z
dc.description.abstractCortical inhibitory interneurons form a broad spectrum of subtypes. This diversity suggests a division of labor, in which each cell type supports a distinct function. In the present era of optimisation-based algorithms, it is tempting to speculate that these functions were the evolutionary or developmental driving force for the spectrum of interneurons we see in the mature mammalian brain. In this study, we evaluated this hypothesis using the two most common interneuron types, parvalbumin (PV) and somatostatin (SST) expressing cells, as examples. PV and SST interneurons control the activity in the cell bodies and the apical dendrites of excitatory pyramidal cells, respectively, due to a combination of anatomical and synaptic properties. But was this compartment-specific inhibition indeed the function for which PV and SST cells originally evolved? Does the compartmental structure of pyramidal cells shape the diversification of PV and SST interneurons over development? To address these questions, we reviewed and reanalyzed publicly available data on the development and evolution of PV and SST interneurons on one hand, and pyramidal cell morphology on the other. These data speak against the idea that the compartment structure of pyramidal cells drove the diversification into PV and SST interneurons. In particular, pyramidal cells mature late, while interneurons are likely committed to a particular fate (PV vs. SST) during early development. Moreover, comparative anatomy and single cell RNA-sequencing data indicate that PV and SST cells, but not the compartment structure of pyramidal cells, existed in the last common ancestor of mammals and reptiles. Specifically, turtle and songbird SST cells also express the Elfn1 and Cbln4 genes that are thought to play a role in compartment-specific inhibition in mammals. PV and SST cells therefore evolved and developed the properties that allow them to provide compartment-specific inhibition before there was selective pressure for this function. This suggest that interneuron diversity originally resulted from a different evolutionary driving force and was only later co-opted for the compartment-specific inhibition it seems to serve in mammals today. Future experiments could further test this idea using our computational reconstruction of ancestral Elfn1 protein sequences.
dc.identifier.eissn1662-5110
dc.identifier.urihttps://depositonce.tu-berlin.de/handle/11303/19200
dc.identifier.urihttps://doi.org/10.14279/depositonce-17996
dc.language.isoen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
dc.subject.ddc600 Technik, Medizin, angewandte Wissenschaften::610 Medizin und Gesundheit::610 Medizin und Gesundheit
dc.subject.otherinhibition
dc.subject.otherinterneuron
dc.subject.otherevolution
dc.subject.otherdevelopment
dc.subject.othermicrocircuits
dc.subject.othersingle cell RNA seq
dc.subject.otherneural morphology
dc.subject.otherpyramidal cell dendrites
dc.titleCortical interneurons: fit for function and fit to function? Evidence from development and evolution
dc.typeArticle
dc.type.versionpublishedVersion
dcterms.bibliographicCitation.articlenumber1172464
dcterms.bibliographicCitation.doi10.3389/fncir.2023.1172464
dcterms.bibliographicCitation.journaltitleFrontiers in Neural Circuits
dcterms.bibliographicCitation.originalpublishernameFrontiers
dcterms.bibliographicCitation.originalpublisherplaceLausanne
dcterms.bibliographicCitation.volume17
dcterms.rightsHolder.referenceCreative-Commons-Lizenz
tub.accessrights.dnbfree
tub.affiliationFak. 4 Elektrotechnik und Informatik::Inst. Softwaretechnik und Theoretische Informatik::FG Modellierung kognitiver Prozesse
tub.publisher.universityorinstitutionTechnische Universität Berlin

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