Using voltage‐sensitive dye recording to image the functional development of neuronal circuits in vertebrate embryos

Glover, Joel C.; Sato, Katsushige; Momose‐Sato, Yoko

doi:10.1002/dneu.20629

Cited by 32 publications

(18 citation statements)

References 57 publications

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“…The neonatal mouse is amenable to a combination of molecular, genetic, anatomical, physiological, and behavioral approaches to the elucidation of neuronal network organization. In particular, because of its small size and the possibility to use highly tractable ex vivo preparations, it is highly amenable to electrophysiological approaches [33], rapid and precise tract-tracing [34] and high-throughput optical recording approaches that permit the dynamic assessment of functional synaptic connections onto large numbers of spinal neurons simultaneously [29]–[32], [35], [36].…”

Section: Introductionmentioning

confidence: 99%

A Neonatal Mouse Spinal Cord Injury Model for Assessing Post-Injury Adaptive Plasticity and Human Stem Cell Integration

et al. 2013

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Despite limited regeneration capacity, partial injuries to the adult mammalian spinal cord can elicit variable degrees of functional recovery, mediated at least in part by reorganization of neuronal circuitry. Underlying mechanisms are believed to include synaptic plasticity and collateral sprouting of spared axons. Because plasticity is higher in young animals, we developed a spinal cord compression (SCC) injury model in the neonatal mouse to gain insight into the potential for reorganization during early life. The model provides a platform for high-throughput assessment of functional synaptic connectivity that is also suitable for testing the functional integration of human stem and progenitor cell-derived neurons being considered for clinical cell replacement strategies. SCC was generated at T9–T11 and functional recovery was assessed using an integrated approach including video kinematics, histology, tract tracing, electrophysiology, and high-throughput optical recording of descending inputs to identified spinal neurons. Dramatic degeneration of axons and synaptic contacts was evident within 24 hours of SCC, and loss of neurons in the injured segment was evident for at least a month thereafter. Initial hindlimb paralysis was paralleled by a loss of descending inputs to lumbar motoneurons. Within 4 days of SCC and progressively thereafter, hindlimb motility began to be restored and descending inputs reappeared, but with examples of atypical synaptic connections indicating a reorganization of circuitry. One to two weeks after SCC, hindlimb motility approached sham control levels, and weight-bearing locomotion was virtually indistinguishable in SCC and sham control mice. Genetically labeled human fetal neural progenitor cells injected into the injured spinal cord survived for at least a month, integrated into the host tissue and began to differentiate morphologically. This integrative neonatal mouse model provides opportunities to explore early adaptive plasticity mechanisms underlying functional recovery as well as the capacity for human stem cell-derived neurons to integrate functionally into spinal circuits.

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Section: Introductionmentioning

confidence: 99%

A Neonatal Mouse Spinal Cord Injury Model for Assessing Post-Injury Adaptive Plasticity and Human Stem Cell Integration

et al. 2013

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“…Voltage-sensitive indicators on the other hand provide direct information about changes in membrane potential irrespective of the cause and the sign, permitting the assessment of both excitatory and inhibitory synaptic interactions and depolarizing and hyperpolarizing neurotransmitter and drug effects. 92, 93 …”

Section: Altered Neuronal Cell Biology and Functionmentioning

confidence: 99%

Modeling psychiatric disorders: from genomic findings to cellular phenotypes

et al. 2016

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Major programs in psychiatric genetics have identified >150 risk loci for psychiatric disorders. These loci converge on a small number of functional pathways, which span conventional diagnostic criteria, suggesting a partly common biology underlying schizophrenia, autism and other psychiatric disorders. Nevertheless, the cellular phenotypes that capture the fundamental features of psychiatric disorders have not yet been determined. Recent advances in genetics and stem cell biology offer new prospects for cell-based modeling of psychiatric disorders. The advent of cell reprogramming and induced pluripotent stem cells (iPSC) provides an opportunity to translate genetic findings into patient-specific in vitro models. iPSC technology is less than a decade old but holds great promise for bridging the gaps between patients, genetics and biology. Despite many obvious advantages, iPSC studies still present multiple challenges. In this expert review, we critically review the challenges for modeling of psychiatric disorders, potential solutions and how iPSC technology can be used to develop an analytical framework for the evaluation and therapeutic manipulation of fundamental disease processes.

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“…We have applied optical techniques to the embryonic nervous system and established the feasibility of using VSD recording to analyze neuronal activity in the peripheral and central nervous systems (CNSs) (for reviews see Momose-Sato et al, 2001, 2002; Glover et al, 2008; Momose-Sato & Sato, 2011). The physiological approach to the embryonic nervous system has been greatly advanced by the optical technique because conventional electrophysiological measurements are technically difficult or impossible in the early developing CNS, in which the cells are small and fragile.…”

Section: Introductionmentioning

confidence: 99%

Evaluation of Voltage-Sensitive Fluorescence Dyes for Monitoring Neuronal Activity in the Embryonic Central Nervous System

et al. 2013

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Using an optical imaging technique with voltage-sensitive dyes (VSDs), we have been investigating the functional organization and architecture of the central nervous system (CNS) during embryogenesis. In the embryonic nervous system, a merocyanine-rhodanine dye, NK2761, has proved to be the most useful absorption dye for detecting neuronal activity because of its high signal-to-noise ratio (S/N), low toxicity, and small dye bleaching. In the present study, we evaluated the suitability of voltage-sensitive fluorescence dyes for optical recording in the embryonic CNS. We screened eight styryl (hemicyanine) dyes in isolated brainstem-spinal cord preparations from 7-day old chick embryos. Measurements of voltage-related optical signals were made using a multiple-site optical recording system. The signal size, S/N, photobleaching, effects of perfusion, and recovery of neural responses after staining were compared. We also evaluated optical responses with various magnifications. Although the S/N was lower than with the absorption dye, clear optical responses were detected with several fluorescence dyes, including di-2-ANEPEQ, di-4-ANEPPS, di-3-ANEPPDHQ, di-4-AN(F)EPPTEA, di-2-AN(F)EPPTEA, and di-2-ANEPPTEA. Di-2-ANEPEQ showed the largest S/N, whereas its photobleaching was faster and the recovery of neural responses after staining was slower. Di-4-ANEPPS and di-3-ANEPPDHQ also exhibited a large S/N, but required a relatively long time for recovery of neural activity. Di-4-AN(F)EPPTEA, di-2-AN(F)EPPTEA, and di-2-ANEPPTEA showed smaller S/Ns than di-2-ANEPEQ, di-4-ANEPPS, and di-3-ANEPPDHQ, but the recovery of neural responses after staining was faster. This study demonstrates the potential utility of these styryl dyes in optical monitoring of voltage changes in the embryonic CNS.

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Using voltage‐sensitive dye recording to image the functional development of neuronal circuits in vertebrate embryos

Cited by 32 publications

References 57 publications

A Neonatal Mouse Spinal Cord Injury Model for Assessing Post-Injury Adaptive Plasticity and Human Stem Cell Integration

A Neonatal Mouse Spinal Cord Injury Model for Assessing Post-Injury Adaptive Plasticity and Human Stem Cell Integration

Modeling psychiatric disorders: from genomic findings to cellular phenotypes

Evaluation of Voltage-Sensitive Fluorescence Dyes for Monitoring Neuronal Activity in the Embryonic Central Nervous System

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