Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal mouse somatosensory cortex

Subplate neurons (SPNs) are thought to play a role in nascent sensory processing in neocortex. To better understand how heterogeneity within this population relates to emergent function, we investigated the synaptic connectivity of Lpar1-EGFP SPNs through the first postnatal week in whisker somatosensory cortex (S1BF). These SPNs comprise of two morphological subtypes: fusiform SPNs with local axons, and pyramidal SPNs with axons that extend through the marginal zone. The former receive translaminar synaptic input up until the emergence of the whisker barrels; a timepoint coincident with significant cell death. In contrast, pyramidal SPNs receive local input from the subplate at early ages but then – during the later time window, acquire input from overlying cortex. Combined electrical and optogenetic activation of thalamic afferents identified that Lpar1-EGFP SPNs receive sparse thalamic innervation. These data reveal components of the postnatal network that interpret sparse thalamic input to direct the emergent columnar structure of S1BF.

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Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal somatosensory cortex

10.1101/2020.05.12.088450 ◽

2020 ◽

Author(s):

Filippo Ghezzi ◽

Andre Marques-Smith ◽

Paul Anastasiades ◽

Daniel Lyngholm ◽

Cristiana Vagnoni ◽

...

Keyword(s):

Somatosensory Cortex ◽

Laser Scanning ◽

Columnar Structure ◽

Neuronal Population ◽

Early Postnatal Development ◽

Thalamic Input ◽

Subplate Neurons ◽

Caged Glutamate ◽

Laser Scanning Photostimulation ◽

Local Input

ABSTRACTSubplate 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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Hippocampal neurons with stable excitatory connectivity become part of neuronal representations

PLoS Biology ◽

10.1371/journal.pbio.3000928 ◽

2020 ◽

Vol 18 (11) ◽

pp. e3000928 ◽

Cited By ~ 2

Author(s):

Tim P. Castello-Waldow ◽

Ghabiba Weston ◽

Alessandro F. Ulivi ◽

Alireza Chenani ◽

Yonatan Loewenstein ◽

...

Keyword(s):

Hippocampal Neurons ◽

Pyramidal Neurons ◽

Time Window ◽

Structural Connectivity ◽

Time Lapse ◽

Early Gene ◽

Synaptic Connectivity ◽

Time Duration ◽

Hippocampal Ca1 ◽

Cornu Ammonis

Experiences are represented in the brain by patterns of neuronal activity. Ensembles of neurons representing experience undergo activity-dependent plasticity and are important for learning and recall. They are thus considered cellular engrams of memory. Yet, the cellular events that bias neurons to become part of a neuronal representation are largely unknown. In rodents, turnover of structural connectivity has been proposed to underlie the turnover of neuronal representations and also to be a cellular mechanism defining the time duration for which memories are stored in the hippocampus. If these hypotheses are true, structural dynamics of connectivity should be involved in the formation of neuronal representations and concurrently important for learning and recall. To tackle these questions, we used deep-brain 2-photon (2P) time-lapse imaging in transgenic mice in which neurons expressing the Immediate Early Gene (IEG) Arc (activity-regulated cytoskeleton-associated protein) could be permanently labeled during a specific time window. This enabled us to investigate the dynamics of excitatory synaptic connectivity—using dendritic spines as proxies—of hippocampal CA1 (cornu ammonis 1) pyramidal neurons (PNs) becoming part of neuronal representations exploiting Arc as an indicator of being part of neuronal representations. We discovered that neurons that will prospectively express Arc have slower turnover of synaptic connectivity, thus suggesting that synaptic stability prior to experience can bias neurons to become part of representations or possibly engrams. We also found a negative correlation between stability of structural synaptic connectivity and the ability to recall features of a hippocampal-dependent memory, which suggests that faster structural turnover in hippocampal CA1 might be functional for memory.

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The Balance Between Excitation And Inhibition And Functional Sensory Processing In The Somatosensory Cortex

International Review of Neurobiology - Translating Mechanisms Orofacial Neurological Disorder ◽

10.1016/b978-0-12-385198-7.00012-6 ◽

2011 ◽

pp. 305-333 ◽

Cited By ~ 23

Author(s):

Zhi Zhang ◽

Qian-Quan Sun

Keyword(s):

Somatosensory Cortex ◽

Sensory Processing

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Developmental cell death regulates lineage-related interneuron-oligodendroglia functional clusters and oligodendrocyte homeostasis

Nature Communications ◽

10.1038/s41467-019-11904-4 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 6

Author(s):

David Orduz ◽

Najate Benamer ◽

Domiziana Ortolani ◽

Eva Coppola ◽

Lisa Vigier ◽

...

Keyword(s):

Cell Death ◽

Precursor Cells ◽

Synaptic Connectivity ◽

Gabaergic Interneurons ◽

Oligodendrocyte Precursor Cells ◽

Related Cell ◽

Neuronal Inhibition ◽

Embryonic Origin ◽

Oligodendrocyte Precursor ◽

Developmental Cell Death

Abstract The first wave of oligodendrocyte precursor cells (firstOPCs) and most GABAergic interneurons share common embryonic origins. Cortical firstOPCs are thought to be replaced by other OPC populations shortly after birth, maintaining a consistent OPC density and making postnatal interactions between firstOPCs and ontogenetically-related interneurons unlikely. Challenging these ideas, we show that a cortical firstOPC subpopulation survives and forms functional cell clusters with lineage-related interneurons. Favored by a common embryonic origin, these clusters display unexpected preferential synaptic connectivity and are anatomically maintained after firstOPCs differentiate into myelinating oligodendrocytes. While the concomitant rescue of interneurons and firstOPCs committed to die causes an exacerbated neuronal inhibition, it abolishes interneuron-firstOPC high synaptic connectivity. Further, the number of other oligodendroglia populations increases through a non-cell-autonomous mechanism, impacting myelination. These findings demonstrate unprecedented roles of interneuron and firstOPC apoptosis in regulating lineage-related cell interactions and the homeostatic oligodendroglia density.

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Layer-specific sensory processing impairment in the primary somatosensory cortex after motor cortex infarction

Scientific Reports ◽

10.1038/s41598-020-60662-7 ◽

2020 ◽

Vol 10 (1) ◽

Cited By ~ 1

Author(s):

Atsushi Fukui ◽

Hironobu Osaki ◽

Yoshifumi Ueta ◽

Kenta Kobayashi ◽

Yoshihiro Muragaki ◽

...

Keyword(s):

Motor Cortex ◽

Somatosensory Cortex ◽

Sensory Processing ◽

Primary Somatosensory Cortex

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Context-Dependent Sensory Processing across Primary and Secondary Somatosensory Cortex

Neuron ◽

10.1016/j.neuron.2020.02.004 ◽

2020 ◽

Vol 106 (3) ◽

pp. 515-525.e5 ◽

Cited By ~ 6

Author(s):

Cameron Condylis ◽

Eric Lowet ◽

Jianguang Ni ◽

Karina Bistrong ◽

Timothy Ouellette ◽

...

Keyword(s):

Somatosensory Cortex ◽

Sensory Processing ◽

Secondary Somatosensory Cortex ◽

Context Dependent

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Dynamic Recording of Cell Death in the In Vitro Dorsal Vagal Nucleus of Rats in Response to Metabolic Arrest

Journal of Neurophysiology ◽

10.1152/jn.00559.2002 ◽

2003 ◽

Vol 89 (1) ◽

pp. 551-561 ◽

Cited By ~ 18

Author(s):

Michael Müller ◽

Klaus Ballanyi

Keyword(s):

Cell Death ◽

Propidium Iodide ◽

Neuronal Death ◽

Time Course ◽

Time Window ◽

Membrane Integrity ◽

Brain Slices ◽

Limited Information ◽

Histological Techniques ◽

Metabolic Arrest

Anoxic/ischemic neuronal death is usually assessed in cell cultures or in vivo within a time window of 24 h to several days using the nucleic acid stain propidium iodide or histological techniques. Accordingly, there is limited information on the time course of such neuronal death. We loaded acute rat brain stem slices with propidium iodide for dynamic fluorometric recording of metabolic arrest-related cell death in the dorsal vagal nucleus. This model was chosen because dorsal vagal neurons show a graded response to metabolic inhibition: anoxia and aglycemia cause a sustained hyperpolarization, whereas ischemia induces a glutamate-mediated, irreversible depolarization. We found that the number of propidium iodide–labeled cells increased from 27% to 43% of total cell count within 1–7 h after preparation of slices. Compared with these untreated control slices, cyanide-induced anoxia (30 min) or aglycemia (1 h) did not cause further cell death, whereas 3-h aglycemia destroyed an additional 13% of cells. Ischemia (1 h) due to cyanide plus iodoacetate immediately labeled an additional 20% of cells, and an additional 48% of cells were destroyed within the following 3 h of postischemia. Continuous recording of propidium iodide fluorescence showed that loss of membrane integrity started within 25 min after onset of the ischemic depolarization and the concomitant intracellular Ca2+ rise. The results show that propidium iodide can be used to monitor cell death in acute brain slices. Our findings suggest that pronounced cell death occurs within a period of 1–4 h after onset of metabolic arrest and is apparently due to necrotic/oncotic mechanisms.

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