Monitoring Population Membrane Potential Signals During Development of the Vertebrate Nervous System

Abstract

The functional organization of the vertebrate central nervous system (CNS) during the early phase of development has long been unclear, because conventional electrophysiological means have several technical limitations. First, early embryonic neurons are small and fragile, and the application of microelectrodes is often difficult. Second, the simultaneous recording of electrical activity from multiple sites is limited, and as a consequence, response patterns of neural networks cannot be assessed. Optical recording techniques with voltage-sensitive dyes have overcome these obstacles and provided a new approach to the analysis of the functional development/organization of the CNS. In this review, we provide detailed information concerning the recording of optical signals in the embryonic nervous system. After outlining methodological considerations, we present examples of recent progress in optical studies on the embryonic nervous system with special emphasis on two topics. The first is the study of how synapse networks form in specific neuronal circuits. The second is the study of non-specific correlated wave activity, which is considered to play a fundamental role in neural development. These studies clearly demonstrate the utility of fast voltage-sensitive dye imaging as a powerful tool for elucidating the functional organization of the vertebrate embryonic CNS.

Oscillations in the embryonic chick olfactory bulb: initial expression and development revealed by optical imaging with a voltage-sensitive dye

“…In the present study, we applied an optical imaging technique with a VSD to embryonic chick N.I–OB–forebrain preparations, and succeeded in recording oscillations in the OB. The VSD imaging technique has made it possible to detect electrophysiological events simultaneously from large populations of cells in preparations (for reviews see Cohen & Salzberg, ; Salzberg, ; Grinvald et al ., ; Wu et al ., ; Zecevic & Antic, ), and also facilitated the physiological analysis of the embryonic CNS that is inaccessible to microelectrodes (for reviews see Momose‐Sato et al ., , ; Glover et al ., ; Momose‐Sato & Sato, ). The optical recording technique has been applied to the olfactory system of various animals (Orbach & Cohen, ; Kauer et al ., ; Cattarelli & Cohen, ; Cinelli & Salzberg, , ; Senseman, ; Litaudon et al ., ,b; Lam et al ., ; Fu et al ., ).…”

“…One was a 1020‐site optical recording system with a 34 × 34‐element silicon photodiode array which was constructed and developed in our laboratory (Hirota et al ., ; Momose‐Sato et al ., , ), and the other was a 464‐site optical recording system with a hexagonally arranged photodiode‐fibre optic camera (NeuroPDA; RedShirtImaging LLC, Fairfield, CT, USA) (Wu & Cohen, ; Wu et al ., ). The methods used for multiple‐site optical recording of electrical activity in the embryonic nervous system are described elsewhere (for reviews see Momose‐Sato et al ., , ). In brief, bright‐field illumination was provided by a 300‐W tungsten–halogen lamp (Type JC‐24V/300W; Kondo Philips Ltd, Tokyo, Japan) driven by a stable DC‐power supply.…”

“…This approach is also indispensable to elucidate when and how the sensory information becomes integrated in the CNS during development. We have previously applied voltage‐sensitive dye (VSD) imaging to chick, rat and mouse embryos, and established its feasibility for monitoring electrical activity from the embryonic CNS (for reviews see Momose‐Sato et al ., , ). We assessed the onset and early development of action potential activity and postsynaptic function related to cranial/spinal nerves (for reviews see Momose‐Sato et al ., , ; Momose‐Sato & Sato, , ; Glover et al ., ).…”

Optical analysis of functional development of the facial motor nucleus in the embryonic rat brainstem

“…The methods used for multiple‐site optical recording of electrical activity in embryonic nervous systems are described in detail elsewhere (for reviews see Momose‐Sato et al., , ). In brief, bright‐field illumination was provided using a 300 W tungsten‐halogen lamp (Type JC‐24V/300W; Kondo Philips Ltd., Tokyo, Japan) driven by a stable DC‐power supply.…”

“…This technique has been used for investigating spatiotemporal patterns of neural activity from a variety of invertebrate and vertebrate central nervous systems (CNSs) (for reviews see Cohen & Salzberg, ; Salzberg, ; Grinvald, Frostig, Lieke, & Hildesheim, ; Canepari, Zecevic, & Bernus, ). In our previous investigations, we established the feasibility of VSD recording for detecting electrical activity from embryonic nervous systems (for reviews see Glover, Sato, & Momose‐Sato, ; Momose‐Sato, Sato, & Kamino, , ; Sato & Momose‐Sato, ). We applied the optical recording technique to the embryonic chick, rat, and mouse CNSs and succeeded in elucidating spatiotemporal patterns and developmental dynamics of neural activity in several sensory and motor nuclei (for reviews see Momose‐Sato et al., ; Momose‐Sato, Sato, & Kamino, ; Momose‐Sato et al., ; Momose‐Sato & Sato, , ).…”