Neocortical Projection Neurons Instruct Inhibitory Interneuron Circuit Development in a Lineage-Dependent Manner

Wester, Jason C.; Mahadevan, Vivek; Rhodes, C. T.; Calvigioni, Daniela; Venkatesh, Sanan; Maric, Dragan; Hunt, Steven; Yuan, Xitong; Zhang, Yajun; Petros, Timothy J.; McBain, Chris J.

doi:10.1016/j.neuron.2019.03.036

Cited by 55 publications

(62 citation statements)

References 106 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…VIP+ interneurons (INs) represent one of the major subtypes of 5-HT 3A R-expressing GABAergic interneuron (Lee et al, 2010;Rudy et al, 2011) that originate from the ventricular zone of the caudal ganglionic eminence (CGE) in the embryonic telencephalon. In line with other CGE-derived INs, VIP+ INs preferentially populate supragranular layers of neocortex within the first postnatal week (Miyoshi and Fishell, 2011) under the control of serotonin (5-HT) (Frazer et al, 2015), the transcription factor Prox1 (Miyoshi et al, 2015), and local cues from pyramidal cells (Wester et al, 2019). Three lines of evidence suggest that VIP+ INs represent a key neuronal population that orchestrates sensory-motor processing and a valid target for our investigation: first, VIP+ INs have been shown to play a key role in integrating local and long range inputs in the mature brain (Lee et al, 2013;Wall et al, 2016;Zhang et al, 2014), despite only comprising a small fraction of the total neuronal population in neocortex (Rudy et al, 2011;Xu et al, 2010).…”

Section: Introductionmentioning

confidence: 64%

“…Our results point to subtle deficits in the layer location and synaptic integration of VIP+ INs within the local S1BF circuit following cell autonomous deletion of Prox1 in VIP+ INs; deficits that have consequences for sensory processing in the juvenile mouse. The selective impact on local connections points to a failure of VIP+ INs to appropriately interpret normal columnar signals for synaptic integration (Miyoshi et al, 2015;Wester et al, 2019) following deletion of this transcription factor. Altered molecular machinery could include members of the neurexin -neuroligin synaptic organizer protein family that are selectively expressed by Prox1+ INs (Lukacsovich et al, 2019), and have the ability to differentially regulate local versus long-range glutamatergic connections (Pregno et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Ontogeny of the VIP+ interneuron sensory-motor circuit prior to active whisking

Vagnoni

Baruchin

Ghezzi

et al. 2020

Preprint

View full text Add to dashboard Cite

ABSTRACTDevelopment of the cortical circuits for sensory-motor processing require the coordinated integration of both columnar and long-range synaptic connections. To understand how this occurs at the level of individual neurons we have explored the timeline over which vasoactive intestinal peptide (VIP)-expressing interneurons integrate into mouse somatosensory cortex. We find a distinction in emergent long-range anterior-motor and columnar glutamatergic inputs onto layer (L)2 and L3 VIP+ interneurons respectively. In parallel, VIP+ interneurons form efferent connections onto both pyramidal cells and interneurons in the immediate column in an inside-out manner. Cell-autonomous deletion of the fate-determinant transcription factor, Prox1, spares long-range anterior-motor inputs onto VIP+ interneurons, but leads to deficits in local connectivity. This imbalance in the somatosensory circuit results in altered spontaneous and sensory-evoked cortical activity in vivo. This identifies a critical role for VIP+ interneurons, and more broadly interneuron heterogeneity, in formative circuits of neocortex.

show abstract

Section: Introductionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 99%

Ontogeny of the VIP+ interneuron sensory-motor circuit prior to active whisking

Vagnoni

Baruchin

Ghezzi

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…2c). These results suggest that interneurons acquire region-specific components of their molecular identities (see also 24,25 ), and that these details are shared across species and most strongly among close relatives.…”

Section: Introductionmentioning

confidence: 84%

Innovations in Primate Interneuron Repertoire

Krienen

Goldman

Zhang

et al. 2019

Preprint

View full text Add to dashboard Cite

26Primates and rodents, which descended from a common ancestor more than 90 million years 27 ago, exhibit profound differences in behavior and cognitive capacity. Modifications, 28 specializations, and innovations to brain cell types may have occurred along each lineage. We 29 used Drop-seq to profile RNA expression in more than 184,000 individual telencephalic 30 interneurons from humans, macaques, marmosets, and mice. Conserved interneuron types 31 varied significantly in abundance and RNA expression between mice and primates, but varied 32 much more modestly among primates. In adult primates, the expression patterns of dozens of 33 genes exhibited spatial expression gradients among neocortical interneurons, suggesting that 34 adult neocortical interneurons are imprinted by their local cortical context. In addition, we found 35 that an interneuron type previously associated with the mouse hippocampus-the "ivy cell", which 36 has neurogliaform characteristics-has become abundant across the neocortex of humans, 37 macaques, and marmosets. The most striking innovation was subcortical: we identified an 38 abundant striatal interneuron type in primates that had no molecularly homologous cell population 39 in mouse striatum, cortex, thalamus, or hippocampus. These interneurons, which expressed a 40 unique combination of transcription factors, receptors, and neuropeptides, including the 41 neuropeptide TAC3, constituted almost 30% of striatal interneurons in marmosets and humans. 42Understanding how gene and cell-type attributes changed or persisted over the evolutionary 43 divergence of primates and rodents will guide the choice of models for human brain disorders and 44 mutations and help to identify the cellular substrates of expanded cognition in humans and other 45 primates. 46 47 53 54 Brain structures, circuits, and cell types have acquired adaptations and new functions along 55 specific evolutionary lineages. Numerous examples of modifications to specific cell types within 56 larger conserved brain systems have been discovered, including hindbrain circuits that control 57 species-specific courtship calls in frogs 3 , the evolution of trichromatic vision in primates 4 , and 58 neurons that have converted from motor to sensory processing to produce a novel swimming 59 behavior in sand crabs 5 . Evolution can modify brain structures through a wide range of 60 mechanisms, including increasing or reducing production of cells of a given type, altering the 61 molecular and cellular properties of shared cell types, reallocating or redeploying cell types to 62 new locations in the brain, or inventing entirely new cell types (Fig. 1a). 63 64 Single-cell RNA sequencing, which systematically measures gene expression in thousands of 65 individual cells, has recently enabled detailed comparisons of cell types and expression patterns 66 between homologous brain structures separated by millions of years of evolution 4,6,7 (non-single 67 cell approaches have also yielded important insights in this domain, e.g. 8 ). For example...

show abstract

“…The cellular sources of these cell-extrinsic signals are likely to be diverse. Among the most studied, PNs located in deep and superficial cortical layers regulate the differential laminar distribution of cortical INs Lodato et al 2011;Wester et al 2019), but the molecular mechanisms through which distinct sets of PNs control the allocation of different types of cortical INs into specific cortical layers remains quite unexplored. It has been proposed that INs and PNs, eventually paired into cortical circuits, express complementary molecules which ultimately control the lamination of INs.…”

Section: Sema3a As a Cue Regulating The Allocation Of Cortical Hinsmentioning

confidence: 99%

“…In addition to these cell-intrinsic mechanisms, glutamatergic projection neurons (PNs) are able to influence the lamination of cortical INs. Namely, ectopic deep layer PNs can recruit LHX6 + INs (Lodato et al 2011), while Satb2-expressing interhemispheric PNs from the visual cortex control cortical integration of hINs (Wester et al 2019). How PNs settling into the cortical plate attract migrating INs has been well documented for MGE-derived INs (Bartolini et al 2017) but the molecular mechanisms that regulate their laminar allocation is yet poorly elucidated.…”

Section: Introductionmentioning

confidence: 99%

PlexinA4-Semaphorin3A mediated crosstalk between main cortical interneuron classes is required for superficial interneurons lamination

Limoni

Niquille

Murthy

et al. 2020

Preprint

View full text Add to dashboard Cite

In the mammalian cerebral cortex, the developmental events governing the allocation of different classes of inhibitory interneurons (INs) into distinct cortical layers are poorly understood. Here we report that the guidance receptor PlexinA4 (PLXNA4) is upregulated in serotonin receptor 3a-expressing (HTR3A + ) cortical INs (hINs) as they invade the cortical plate and that it regulates their laminar allocation to superficial cortical layers. We find that the PLXNA4 ligand Semaphorin3A (SEMA3A) acts as a chemorepulsive factor on hINs migrating into the nascent cortex and demonstrate that SEMA3A specifically controls their laminar positioning through PLXNA4. We identify that deep layer INs constitute a major source of SEMA3A in the developing cortex and demonstrate that cell-type specific genetic deletion of SEMA3A in these INs specifically affects the laminar allocation of hINs. These data demonstrate that in the neocortex, deep layer INs control the laminar allocation of hINs into superficial layers.

show abstract

Neocortical Projection Neurons Instruct Inhibitory Interneuron Circuit Development in a Lineage-Dependent Manner

Cited by 55 publications

References 106 publications

Ontogeny of the VIP+ interneuron sensory-motor circuit prior to active whisking

Ontogeny of the VIP+ interneuron sensory-motor circuit prior to active whisking

Innovations in Primate Interneuron Repertoire

PlexinA4-Semaphorin3A mediated crosstalk between main cortical interneuron classes is required for superficial interneurons lamination

Contact Info

Product

Resources

About