Layer 6b Is Driven by Intracortical Long-Range Projection Neurons

Zolnik, Timothy A.; Ledderose, Julia; Toumazou, Maria; Trimbuch, Thorsten; Oram, Tess; Rosenmund, Christian; Eickholt, Britta J.; Sachdev, Robert N. S.; Larkum, Matthew E.

doi:10.1016/j.celrep.2020.02.044

Cited by 61 publications

(78 citation statements)

References 90 publications

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“…The remaining pyramidal SPNs are evenly split between those that are still dominated by local inputs and those that acquire an array of diverse inputs from across cortical layers, located both in the immediate and adjacent cortical columns. This diversification of synaptic input fits with the rapid transition to columnar signalling previously reported at P5 25 , and suggests that this time point represents the switch from transient SP to layer 6b (L6b) 13 in S1BF. Our study identifies that Lpar1-EGFP SPNs in S1BF have an additional novel function that does not conform to the canonical model for SPNs established across sensory cortices, wherein SPNs act as relay cells for thalamic input to L4 1,4,38 .…”

Section: Discussionsupporting

confidence: 86%

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Non-canonical role forLpar1-EGFPsubplate neurons in early postnatal somatosensory cortex

Ghezzi

Marques-Smith

Anastasiades

et al. 2020

Preprint

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Subplate neurons (SPNs) are a transient neuronal population shown to play a key role in nascent sensory processing relaying thalamic information to the developing cerebral cortex.However there is little understanding of how heterogeneity within this population relates to emergent function. To address this question we employed optical and electrophysiological technologies to investigate the synaptic connectivity of SPNs defined by expression of the Lpar1-EGFP transgene through the first postnatal week in primary whisker somatosensory cortex (S1BF) in mouse. Our data identify that the Lpar1-EGFP SPNs represent two morphological subtypes: (1) transient, fusiform SPNs with axons largely restricted to the subplate zone; (2) pyramidal SPNs with axon collaterals that traverse the overlying cortex to extend through the marginal zone. Laser scanning photostimulation of caged glutamate was used to determine columnar glutamatergic and GABAergic input onto both of these SPN subtypes. These experiments revealed that the former receive translaminar input from more superficial cortical layers up until the emergence of the whisker barrels (~postnatal (P)5). In contrast, pyramidal SPNs only receive local input from the adjacent subplate network at early ages but then at later ages can acquire varied input from the overlying cortex.Combined electrical stimulation of the ventral posterior nucleus of the thalamus and optogenetic activation of thalamic afferents in thalamocortical slice preparations revealed that Lpar1-EGFP SPNs only receive sparse thalamic innervation during early postnatal development. Taken together, these data reveal two components of the postnatal network that interpret sparse thalamic input to direct the emergent columnar structure of neonatal somatosensory cortex.

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Section: Discussionsupporting

confidence: 86%

“…A large proportion of SPNs disappear during the first postnatal week in the mouse cortex 7 . SPNs that do not undergo programmed cell death continue to form a thin , compact sublayer of layer 6, termed layer (L)6b in mature neocortex 12,13 . Layer 6b can be cytoarchitectonically distinguished from embryonic stages.…”

Section: Introductionmentioning

confidence: 99%

Non-canonical role forLpar1-EGFPsubplate neurons in early postnatal somatosensory cortex

Ghezzi

Marques-Smith

Anastasiades

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…Moreover, corticofugal projections from L6b to POm have also been confirmed (Bourassa et al 1995;Hoerder-Suabedissen et al 2018). L6b receives substantial innervation from the contralateral sensorimotor cortical areas producing a contralateral drive to this layer (Zolnik et al 2020). Here, we found that VPM did not respond to ipsilateral stimuli.…”

Section: Pom Mediates Bilateral Sensory Processing Pom Integration Ofsupporting

confidence: 71%

“…14A). Consistent with this idea, it is known that motor and S2 cortical regions elicited strong direct input to L6b and L5 in S1 (Mao et al 2011;Zolnik et al, 2020). Moreover, corticofugal projections from L6b to POm have also been confirmed (Bourassa et al 1995;Hoerder-Suabedissen et al 2018).…”

Section: Pom Mediates Bilateral Sensory Processing Pom Integration Ofsupporting

confidence: 54%

Thalamic encoding of complex sensory patterns and its possible role in cognition

Castejon

Martín-Cortecero

Núñez

2020

Preprint

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The function of the higher-order sensory thalamus remains unresolved. Here, POm nucleus was examined by in vivo extracellular recordings across a range of complex sensory patterns. We found that POm was highly sensitive to multiwhisker stimuli involving complex spatiotemporal interactions. The dynamical spatiotemporal structure of sensory patterns and the different complexity of their parts was accurately reflected in precise POm activity changes. Importantly, POm was also able to respond to ipsilateral stimulation and was implicated in the representation of bilateral tactile events by integrating simultaneous signals arising from both whisker pads. We found that POm nuclei are mutually connected through the cortex forming a functional POm-POm loop. We unravelled the nature and content of the messages travelling through this loop showing that they were "structured patterns of sustained activity". These structured messages were transmitted preserving their integrated structure. The implication of different cortical areas was investigated revealing that S1 plays a protagonist role in this functional loop. Our results also demonstrated different laminar implication in the processing of sustained activity in this cortical area and its transmission between hemispheres. We propose a theoretical model in which these "structured patterns of sustained activity" generated by POm may play important roles in perceptual, motor and cognitive functions. From a functional perspective, this proposal, supported by the results described here, provides a novel theoretical framework to understand the implication of the thalamus in cognition. In addition, a profound difference was found between VPM and POm functioning. The hypothesis of Complementary Components is proposed here to explain it.

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“…Some of these connections are remodeled during development, but in the adult mouse there are extensive connections maintained from Layer 6b to local and distant cortical areas, and to thalamus (Hoerder‐Suabedissen et al, 2018). Layer 6b also receives input from thalamus as well as ipsi‐ and contra‐lateral cortical areas (but mostly Layer 5) in S1 (Zolnik et al, 2020) and in V1 and M1 (Szabó, Berry, Hoerder‐Suabedissen, Sharott, Molnár, unpublished).…”

Section: Introductionmentioning

confidence: 99%

In search of common developmental and evolutionary origin of the claustrum and subplate

Bruguier

Suárez

Manger

et al. 2020

J of Comparative Neurology

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The human claustrum, a major hub of widespread neocortical connections, is a thin, bilateral sheet of gray matter located between the insular cortex and the striatum. The subplate is a largely transient cortical structure that contains some of the earliest generated neurons of the cerebral cortex and has important developmental functions to establish intra-and extracortical connections. In human and macaque some subplate cells undergo regulated cell death, but some remain as interstitial white matter cells. In mouse and rat brains a compact layer is formed, Layer 6b, and it remains underneath the cortex, adjacent to the white matter. Whether Layer 6b in rodents is homologous to primate subplate or interstitial white matter cells is still debated. Gene expression patterns, such as those of Nurr1/Nr4a2, have suggested that the rodent subplate and the persistent subplate cells in Layer 6b and the claustrum might have similar origins. Moreover, the birthdates of the claustrum and Layer 6b are similarly precocious in mice. These observations prompted our speculations on the common developmental and evolutionary origin of the claustrum and the subplate. Here we systematically compare the currently available data on cytoarchitecture, evolutionary origin, gene expression, cell types, birthdates, neurogenesis, lineage and migration, circuit connectivity, and cell death of the neurons that contribute to the claustrum and subplate. Based on their similarities and differences we propose a partially common early evolutionary origin of the cells that become claustrum and subplate, a likely scenario that is shared in these cell populations across all amniotes.

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Layer 6b Is Driven by Intracortical Long-Range Projection Neurons

Cited by 61 publications

References 90 publications

Non-canonical role forLpar1-EGFPsubplate neurons in early postnatal somatosensory cortex

Non-canonical role forLpar1-EGFPsubplate neurons in early postnatal somatosensory cortex

Thalamic encoding of complex sensory patterns and its possible role in cognition

In search of common developmental and evolutionary origin of the claustrum and subplate

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