Advertisement

Monitoring Population Membrane Potential Signals During Functional Development of Neuronal Circuits in Vertebrate Embryos

  • Yoko Momose-Sato
  • Katsushige Sato
  • Kohtaro Kamino
Chapter

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 chapter, 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 wfith 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 nonspecific 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.

Keywords

Optical Signal Correlate Activity Optical Recording Intrinsic Signal Transmitted Light Intensity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank Joel C. Glover, Akihiko Hirota, Tetsuro Sakai, Hitoshi Komuro, Yusuke Katoh, Yang Xue-Song, Yoshiyasu Arai, Hiraku Mochida, Itaru Yazawa, Shinichi Sasaki, Toshihisa Tanaka, Naohisa Miyakawa, and Masae Kinoshita for their contribution in the experiments. We express our gratitude to Drs. Lowrence B. Cohen and Brian M. Salzberg for discussions throughout the course of our work and critical reading of the manuscript. We also thank Dr. Shigeo Yasui and Hayashibara Biochemical Laboratories/Kankoh-Shikiso Kenkyusho for synthesizing many dyes including NK2761 at our request. The present study was supported by grants from the Ministry of Education-Science-Culture of Japan and the HFSP, and research funds from the Astellas Foundation for Research on Metabolic Disorders.

References

  1. Abadie V, Champagnat J, Fortin G (2000) Branchiomotor activities in mouse embryo. NeuroReport 11:141–145.PubMedCrossRefGoogle Scholar
  2. Al-Ghoul WM, Miller MW (1993) Development of the principal sensory nucleus of the trigeminal nerve of the rat and evidence for a transient synaptic field in the trigeminal sensory tract. J Comp Neurol 330:476–490.PubMedCrossRefGoogle Scholar
  3. Arai Y, Momose-Sato Y, Sato K, Kamino K (1999) Optical mapping of neural network activity in chick spinal cord at an intermediate stage of embryonic development. J Neurophysiol 81:1889–1902.PubMedGoogle Scholar
  4. Arai Y, Mentis GZ, Wu J-Y, O’Donovan MJ (2007) Ventrolateral origin of each cycle of rhythmic activity generated by the spinal cord of the chick embryo. PLoS One 2(5):e417.PubMedCrossRefGoogle Scholar
  5. Asako M, Doi T, Matsumoto A, Yang S-M, Yamashita T (1999) Spatial and temporal patterns of evoked neural activity from auditory nuclei in chick brainstem detected by optical recording. Acta Otolaryngol 119:900–904.PubMedCrossRefGoogle Scholar
  6. Ben-Ari Y (2001) Developing networks play a similar melody. Trend Neurosci 24:353–359.PubMedCrossRefGoogle Scholar
  7. Ben-Ari Y, Gaiarsa J-L, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87:1215–1284.PubMedCrossRefGoogle Scholar
  8. Bonhoeffer T, Grinvald A (1995) Optical imaging based on intrinsic signals: the methodology. The Weizmann Institute of Science, Israel.Google Scholar
  9. Bonnot A, Mentis GZ, Skoch J, O’Donovan MJ (2005) Electroporation loading of calcium-sensitive dyes into the CNS. J Neurophysiol 93:1793–1808.PubMedCrossRefGoogle Scholar
  10. Chatonnet F, Thoby-Brisson M, Abadie V et al (2002) Early development of respiratory rhythm generation in mouse and chick. Respir Physiol Neurobiol 131:5–13.PubMedCrossRefGoogle Scholar
  11. Cohen LB, Lesher S (1986) Optical monitoring of membrane potential: methods of multisite optical measurement. In: De Weer P, Salzberg BM (eds) Optical methods in cell physiology. Wiley, New York, pp 71–99.Google Scholar
  12. Cohen LB, Salzberg BM (1978) Optical measurement of membrane potential. Rev Physiol Biochem Pharmacol 83:35–88.PubMedGoogle Scholar
  13. Dasheiff RM (1988) Fluorescent voltage-sensitive dyes: applications for neurophysiology. J Clin Neurophysiol 5:211–235.PubMedCrossRefGoogle Scholar
  14. Demarque M, Represa A, Becq H et al (2002) Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36:1051–1061.PubMedCrossRefGoogle Scholar
  15. Demir R, Gao B-X, Jackson MB, Ziskind-Conhaim L (2002) Interactions between multiple rhythm generators produce complex patterns of oscillation in the developing rat spinal cord. J Neurophysiol 87:1094–1105.PubMedGoogle Scholar
  16. Ebner TJ, Chen G (1995) Use of voltage-sensitive dyes and optical recordings in the central nervous system. Prog Neurobiol 46:463–506.PubMedCrossRefGoogle Scholar
  17. Feller MB (1999) Spontaneous correlated activity in developing neural circuits. Neuron 22:653–656.PubMedCrossRefGoogle Scholar
  18. Fortin G, Kato F, Lumsden A, Champagnat J (1995) Rhythm generation in the segmented hindbrain of chick embryos. J Physiol 486:735–744.PubMedGoogle Scholar
  19. Fujii S, Hirota A, Kamino K (1981) Action potential synchrony in embryonic precontractile chick heart: optical monitoring with potentiometric dyes. J Physiol 319:529–541.PubMedGoogle Scholar
  20. Fukuda A, Nabekura J, Ito C, Oomura Y (1987) Development of neuronal properties of rat dorsal motor nucleus of the vagus (DMV). J Physiol Soc Jpn 49:395.Google Scholar
  21. Glover JC, Momose-Sato Y, Sato K (2003) Functional visualization of emerging neural circuits in the brain stem of the chicken embryo using optical recording. In: Abstracts of the 33rd annual meeting of Society for Neuroscience pp 148.Google Scholar
  22. Glover JC, Sato K, Momose-Sato Y (2008) Using voltage-sensitive dye recording to image the functional development of neuronal circuits in vertebrate embryos. Dev Neurobiol 68:804–816.PubMedCrossRefGoogle Scholar
  23. Grinvald A (1985) Real-time optical mapping of neuronal activity: from single growth cones to the intact mammalian brain. Annu Rev Neurosci 8:263–305.PubMedCrossRefGoogle Scholar
  24. Grinvald A, Frostig RD, Lieke E, Hildesheim R (1988) Optical imaging of neuronal activity. Physiol Rev 68:1285–1366.PubMedGoogle Scholar
  25. Hanson MG, Landmesser LT (2003) Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 23:587–600.PubMedGoogle Scholar
  26. Hendricks SJ, Rubel EW, Nishi R (2006) Formation of the avian nucleus magnocellularis from the auditory anlage. J Comp Neurol 498:433–441.PubMedCrossRefGoogle Scholar
  27. Hirota A, Sato K, Momose-Sato Y, Sakai T, Kamino K (1995) A new simultaneous 1020-site optical recording system for monitoring neural activity using voltage-sensitive dyes. J Neurosci Methods 56:187–194.PubMedCrossRefGoogle Scholar
  28. Hume RI, Role LW, Fischbach GD (1983) Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rice membranes. Nature 305:632–634.PubMedCrossRefGoogle Scholar
  29. Hunt PN, McCabe AK, Bosma MM (2005) Midline serotonergic neurons contribute to widespread synchronized activity in embryonic mouse hindbrain. J Physiol 566:807–819.PubMedCrossRefGoogle Scholar
  30. Hunt PN, Gust J, McCabe AK, Bosma MM (2006a) Primary role of the serotonergic midline system in synchronized spontaneous activity during development of the embryonic mouse hindbrain. J Neurobiol 66:1239–1252.PubMedCrossRefGoogle Scholar
  31. Hunt PN, McCabe AK, Gust J, Bosma MM (2006b) Spatial restriction of spontaneous activity towards the rostral primary initiating zone during development of the embryonic mouse hindbrain. J Neurobiol 66:1225–1238.PubMedCrossRefGoogle Scholar
  32. Ikeda K, Onimaru H, Yamada J et al. (2004). Malformation of respiratory–related neuronal activity in Na+, K+-ATPase a2 subunit–deficient mice is attributable to abnormal Cl- homeostasis in brainstem neurons. J Neurosci 24:10693–10701.PubMedCrossRefGoogle Scholar
  33. Kamino K (1991) Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol Rev 71:53–91.PubMedGoogle Scholar
  34. Kamino K, Hirota A, Komuro H (1989a) Optical indications of electrical activity and excitation-contraction coupling in the early embryonic heart. Adv Biophys 25:45–93.PubMedCrossRefGoogle Scholar
  35. Kamino K, Katoh Y, Komuro H, Sato K (1989b) Multiple-site optical monitoring of neural activity evoked by vagus nerve stimulation in the embryonic chick brain stem. J Physiol 409:263–283.PubMedGoogle Scholar
  36. Kamino K, Komuro H, Sakai T, Sato K (1990) Optical assessment of spatially ordered patterns of neural response to vagal stimulation in the embryonic chick brainstem. Neurosci Res 8:255–271.PubMedCrossRefGoogle Scholar
  37. Kamino K, Sakai T, Momose-Sato Y, Hirota A, Sato K (1993) Optical indications of early appearance of postsynaptic potentials in the embryonic chick brain stem. Jpn J Physiol 43(Suppl 1): S43–S51.PubMedGoogle Scholar
  38. Komuro H, Sakai T, Momose-Sato Y, Hirota A, Kamino K (1991) Optical detection of postsynaptic potentials evoked by vagal stimulation in the early embryonic chick brain stem slice. J Physiol 442:631–648.PubMedGoogle Scholar
  39. Komuro H, Momose-Sato Y, Sakai T, Hirota A, Kamino K (1993) Optical monitoring of early appearance of spontaneous membrane potential changes in the embryonic chick medulla oblongata using a voltage-sensitive dye. Neuroscience 52:55–62.PubMedCrossRefGoogle Scholar
  40. Konnerth A, Obaid AL, Salzberg BM (1987) Optical recording of electrical activity from parallel fibres and other cell types in skate cerebellar slices in vitro. J Physiol 393:681–702.PubMedGoogle Scholar
  41. Korn MJ, Cramer KS (2008) Distribution of glial-associated proteins in the developing chick auditory brainstem. Dev Neurobiol 68:1093–1106.PubMedCrossRefGoogle Scholar
  42. Landmesser LT, O’Donovan MJ (1984) Activation patterns of embryonic chick hind limb muscles recorded in ovo and in an isolated spinal cord preparation. J Physiol 347:189–204.PubMedGoogle Scholar
  43. Loew LM (1988) How to choose a potentiometric membrane probe. In: Loew LM (ed) Spectroscopic membrane probes, vol II. CRC Press, Boca Raton, FL, pp 139–151.Google Scholar
  44. Milner LD, Landmesser LT (1999) Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J Neurosci 19:3007–3022.PubMedGoogle Scholar
  45. Miyakawa N, Sato K, Momose-Sato Y (2004) Optical detection of neural function in the chick visual pathway in the early stages of embryogenesis. Eur J Neurosci 20:1133–1149.PubMedCrossRefGoogle Scholar
  46. Mochida H, Sato K, Arai Y et al (2001a) Multiple-site optical recording reveals embryonic organization of synaptic networks in the chick spinal cord. Eur J Neurosci 13:1547–1558.PubMedCrossRefGoogle Scholar
  47. Mochida H, Sato K, Arai Y et al (2001b) Optical imaging of spreading depolarization waves triggered by spinal nerve stimulation in the chick embryo: possible mechanisms for large-scale coactivation of the CNS. Eur J Neurosci 14:809–820.PubMedCrossRefGoogle Scholar
  48. Mochida H, Sato K, Momose-Sato Y (2009) Switching of the transmitters that mediate hindbrain correlated activity in the chick embryo. Eur J Neurosci 29:14–30.PubMedCrossRefGoogle Scholar
  49. Momose-Sato Y, Sato K (2005) Primary vagal projection to the contralateral non-NTS region in the embryonic chick brainstem revealed by optical recording. J Membr Biol 208:183–191.PubMedCrossRefGoogle Scholar
  50. Momose-Sato Y, Sato K (2006) Optical recording of vagal pathway formation in the embryonic brainstem. Auton Neurosci 126–127:39–49.PubMedCrossRefGoogle Scholar
  51. Momose-Sato Y, Komuro H, Sakai T, Hirota A, Kamino K (1991a) Optical monitoring of cholinergic postsynaptic potential in the embryonic chick ciliary ganglion using a voltage-sensitive dye. Biomed Res 12(Suppl 2):139–140.Google Scholar
  52. Momose-Sato Y, Sakai T, Komuro H, Hirota A, Kamino K (1991b) Optical mapping of the early development of the response pattern to vagal stimulation in embryonic chick brain stem. J Physiol 442:649–668.PubMedGoogle Scholar
  53. Momose-Sato Y, Sakai T, Hirota A, Sato K, Kamino K (1993) Optical monitoring of glutaminergic excitatory postsynaptic potentials from the early developing embryonic chick brain stem. Ann N Y Acad Sci 707:454–457.PubMedCrossRefGoogle Scholar
  54. Momose-Sato Y, Sakai T, Hirota A, Sato K, Kamino K (1994) Optical mapping of early embryonic expressions of Mg2+-/APV-sensitive components of vagal glutaminergic EPSPs in the chick brainstem. J Neurosci 14:7572–7584.PubMedGoogle Scholar
  55. Momose-Sato Y, Sato K, Sakai T, Hirota A, Kamino K (1995a) A novel γ-aminobutyric acid response in the embryonic brainstem as revealed by voltage-sensitive dye recording. Neurosci Lett 191:193–196.PubMedCrossRefGoogle Scholar
  56. Momose-Sato Y, Sato K, Sakai T et al (1995b) Evaluation of optimal voltage-sensitive dyes for optical monitoring of embryonic neural activity. J Memb Biol 144:167–176.CrossRefGoogle Scholar
  57. Momose-Sato Y, Sato K, Hirota A, Sakai T, Kamino K (1997) Optical characterization of a novel GABA response in early embryonic chick brainstem. Neuroscience 80:203–219.PubMedCrossRefGoogle Scholar
  58. Momose-Sato Y, Sato K, Hirota A, Kamino K (1998) GABA-induced intrinsic light-scattering changes associated with voltage-sensitive dye signals in embryonic brain stem slices: coupling of depolarization and cell shrinkage. J Neurophysiol 79:2208–2217.PubMedGoogle Scholar
  59. Momose-Sato Y, Sato K, Kamino K (1999a) Optical identification of calcium-dependent action potentials transiently expressed in the embryonic rat brainstem. Neuroscience 90:1293–1310.PubMedCrossRefGoogle Scholar
  60. Momose-Sato Y, Komuro H, Hirota A et al (1999b) Optical imaging of the spatiotemporal patterning of neural responses in the embryonic chick superior cervical ganglion. Neuroscience 90:1069–1083.PubMedCrossRefGoogle Scholar
  61. Momose-Sato Y, Sato K, Kamino K (2001a) Optical approaches to embryonic development of neural functions in the brainstem. Prog Neurobiol 63:151–197.PubMedCrossRefGoogle Scholar
  62. Momose-Sato Y, Sato K, Mochida H et al (2001b) Spreading depolarization waves triggered by vagal stimulation in the embryonic chick brain: optical evidence for intercellular communication in the developing central nervous system. Neuroscience 102:245–262.PubMedCrossRefGoogle Scholar
  63. Momose-Sato Y, Sato K, Kamino K (2002) Application of voltage-sensitive dyes to the embryonic central nervous system. In: Fagan J, Davidson JN, Shimizu N (eds) Recent research developments in membrane biology, vol 1. Research Signpost, Kerara, pp 159–181.Google Scholar
  64. Momose-Sato Y, Miyakawa N, Mochida H, Sasaki S, Sato K (2003a) Optical analysis of depolarization waves in the embryonic brain: a dual network of gap junctions and chemical synapses. J Neurophysiol 89:600–614.PubMedCrossRefGoogle Scholar
  65. Momose-Sato Y, Mochida H, Sasaki S, Sato K (2003b) Depolarization waves in the embryonic CNS triggered by multiple sensory inputs and spontaneous activity: optical imaging with a voltage-sensitive dye. Neuroscience 116:407–423.PubMedCrossRefGoogle Scholar
  66. Momose-Sato Y, Honda Y, Sasaki H, Sato K (2004) Optical mapping of the functional organization of the rat trigeminal nucleus: initial expression and spatiotemporal dynamics of sensory information transfer during embryogenesis. J Neurosci 24:1366–1376.PubMedCrossRefGoogle Scholar
  67. Momose-Sato Y, Honda Y, Sasaki H, Sato K (2005) Optical imaging of large-scale correlated wave activity in the developing rat CNS. J Neurophysiol 94:1606–1622.PubMedCrossRefGoogle Scholar
  68. Momose-Sato Y, Glover J, Sato K (2006) Development of functional synaptic connections in the auditory system visualized with optical recording: afferent-evoked activity is present from early stages. J Neurophysiol 96:1949–1962.PubMedCrossRefGoogle Scholar
  69. Momose-Sato Y, Kinoshita M, Sato K (2007a) Development of vagal afferent projections circumflex to the obex in the embryonic chick brainstem visualized with voltage-sensitive dye recording. Neuroscience 148:140–150.PubMedCrossRefGoogle Scholar
  70. Momose-Sato Y, Kinoshita M, Sato K (2007b) Embryogenetic expression of glossopharyngeal and vagal excitability in the chick brainstem as revealed by voltage-sensitive dye recording. Neurosci Lett 423:138–142.PubMedCrossRefGoogle Scholar
  71. Momose-Sato Y, Sato K, Kinoshita M (2007c) Spontaneous depolarization waves of multiple origins in the embryonic rat CNS. Eur J Neurosci 25:929–944.PubMedCrossRefGoogle Scholar
  72. Momose-Sato Y, Mochida H, Kinoshita M (2009) Origin of the earliest correlated neuronal activity in the chick embryo revealed by optical imaging with voltage-sensitive dyes. Eur J Neurosci 29:1–13.PubMedCrossRefGoogle Scholar
  73. Moody WJ, Bosma MM (2005) Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev 85:883–941.PubMedCrossRefGoogle Scholar
  74. O’Donovan MJ, Ho S, Yee W (1994) Calcium imaging of rhythmic network activity in the developing spinal cord of the chick embryo. J Neurosci 14:6354–6369.PubMedGoogle Scholar
  75. O’Donovan MJ, Bonnot A, Wenner P, Mentis GZ (2005) Calcium imaging of network function in the developing spinal cord. Cell Calcium 37:443–450.PubMedCrossRefGoogle Scholar
  76. O’Donovan MJ, Bonnot A, Mentis GZ et al (2008) Imaging the spatiotemporal organization of neural activity in the developing spinal cord. Dev Neurobiol 68:788–803.PubMedCrossRefGoogle Scholar
  77. Onimaru H, Homma I (2005) Developmental changes in the spatio-temporal pattern of respiratory neuron activity in the medulla of late fetal rat. Neuroscience 131:969–977.PubMedCrossRefGoogle Scholar
  78. Orbach HS, Cohen LB, Grinvald A (1985) Optical mapping of electrical activity in rat somatosensory and visual cortex. J Neurosci 5:1886–1895.PubMedGoogle Scholar
  79. Platel J-C, Boisseau S, Dupuis A et al (2005) Na+ channel-mediated Ca2+ entry leads to glutamate secretion in mouse neocortical preplate. Proc Natl Acad Sci U S A 102:19174–19179.PubMedCrossRefGoogle Scholar
  80. Ren J, Greer JJ (2003) Ontogeny of rhythmic motor patterns generated in the embryonic rat spinal cord. J Neurophysiol 89:1187–1195.PubMedCrossRefGoogle Scholar
  81. Ren J, Momose-Sato Y, Sato K, Greer JJ (2006) Rhythmic neuronal discharge in the medulla and spinal cord of fetal rats in the absence of synaptic transmission. J Neurophysiol 95:527–534.PubMedCrossRefGoogle Scholar
  82. Ross WN, Salzberg BM, Cohen LB et al (1977) Changes in absorption, fluorescence, dichroism, and birefringence in stained giant axons: optical measurement of membrane potential. J Membr Biol 33:141–183.PubMedCrossRefGoogle Scholar
  83. Rubel EW, Fritzsch B (2002) Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25:51–101.PubMedCrossRefGoogle Scholar
  84. Sakai T, Hirota A, Komuro H, Fujii S, Kamino K (1985) Optical recording of membrane potential responses from early embryonic chick ganglia using voltage-sensitive dyes. Brain Res 349:39–51.PubMedGoogle Scholar
  85. Sakai T, Komuro H, Katoh Y et al (1991) Optical determination of impulse conduction velocity during development of embryonic chick cervical vagus nerve bundles. J Physiol 439:361–381.PubMedGoogle Scholar
  86. Salzberg BM (1983) Optical recording of electrical activity in neurons using molecular probes. In: Barker JL, McKelvy JF (eds) Current methods in cellular neurobiology, vol 3, Electrophysiological techniques. Wiley, New York, pp 139–187.Google Scholar
  87. Salzberg BM, Obaid AL, Gainer H (1985) Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis. J Gen Physiol 86:395–411.PubMedCrossRefGoogle Scholar
  88. Sato K, Momose-Sato Y (2003) Optical detection of developmental origin of synaptic function in the embryonic chick vestibulo-cochlear nuclei. J Neurophysiol 89:3215–3224.PubMedCrossRefGoogle Scholar
  89. Sato K, Momose-Sato Y (2004a) Optical detection of convergent projections in the embryonic chick NTS. Neurosci Lett 371:97–101.PubMedCrossRefGoogle Scholar
  90. Sato K, Momose-Sato Y (2004b) Optical mapping reveals developmental dynamics of Mg2+-/APV-sensitive components of glossopharyngeal glutamatergic EPSPs in the embryonic chick NTS. J Neurophysiol 92:2538–2547.PubMedCrossRefGoogle Scholar
  91. Sato K, Momose-Sato Y (2008) Functional organization of the glossopharyngeal and vagus nerve-related nuclei in the embryonic rat brainstem: optical mapping with voltage-sensitive dyes. In: Abstracts of the 38th annual meeting of Society for Neuroscience pp 127.Google Scholar
  92. Sato K, Momose-Sato Y, Sakai T et al (1993) Optical assessment of spatial patterning of strength-duration relationship for vagal responses in the early embryonic chick brainstem. Jpn J Physiol 43:521–539.PubMedCrossRefGoogle Scholar
  93. Sato K, Momose-Sato Y, Sakai T, Hirota A, Kamino K (1995) Responses to glossopharyngeal stimulus in the early embryonic chick brainstem: spatiotemporal patterns in three dimensions from repeated multiple-site optical recording of electrical activity. J Neurosci 15:2123–2140.PubMedGoogle Scholar
  94. Sato K, Momose-Sato Y, Hirota A, Sakai T, Kamino K (1996) Optical studies of the biphasic modulatory effects of glycine on excitatory postsynaptic potentials in the chick brainstem and their embryogenesis. Neuroscience 72:833–846.PubMedCrossRefGoogle Scholar
  95. Sato K, Momose-Sato Y, Arai Y, Hirota A, Kamino K (1997) Optical illustration of glutamate-induced cell swelling coupled with membrane depolarization in embryonic brain stem slices. Neuroreport 8:3559–3563.PubMedCrossRefGoogle Scholar
  96. Sato K, Momose-Sato Y, Hirota A, Sakai T, Kamino K (1998) Optical mapping of neural responses in the embryonic rat brainstem with reference to the early functional organization of vagal nuclei. J Neurosci 18:1345–1362.PubMedGoogle Scholar
  97. Sato K, Momose-Sato Y, Mochida H et al (1999) Optical mapping reveals the functional organization of the trigeminal nuclei in the chick embryo. Neuroscience 93:687–702.PubMedCrossRefGoogle Scholar
  98. Sato K, Yazawa I, Mochida H et al (2000) Optical detection of embryogenetic expression of vagal excitability in the rat brain stem. Neuroreport 11:3759–3763.PubMedCrossRefGoogle Scholar
  99. Sato K, Mochida H, Sasaki S et al (2001) Optical responses to micro-application of GABA agonists in the embryonic chick brain stem. Neuroreport 12:95–98.PubMedCrossRefGoogle Scholar
  100. Sato K, Mochida H, Sasaki S, Momose-Sato Y (2002a) Developmental organization of the glossopharyngeal nucleus in the embryonic chick brainstem slice as revealed by optical sectioning recording. Neurosci Lett 327:157–160.PubMedCrossRefGoogle Scholar
  101. Sato K, Mochida H, Yazawa I, Sasaki S, Momose-Sato Y (2002b) Optical approaches to functional organization of glossopharyngeal and vagal motor nuclei in the embryonic chick hindbrain. J Neurophysiol 88:383–393.PubMedGoogle Scholar
  102. Sato K, Momose-Sato Y, Kamino K (2004a) Light-scattering signals related to neural functions. In: Fagan J, Davidson JN, Shimizu N (eds) Recent research developments in membrane biology, vol 2. Research Signpost, Kerara, pp 21–45.Google Scholar
  103. Sato K, Miyakawa N, Momose-Sato Y (2004b) Optical survey of neural circuit formation in the embryonic chick vagal pathway. Eur J Neurosci 19:1217–1225.PubMedCrossRefGoogle Scholar
  104. Sato K, Kinoshita M, Momose-Sato Y (2007) Optical mapping of spatiotemporal emergence of functional synaptic connections in the embryonic chick olfactory pathway. Neuroscience 144:1334–1346.PubMedCrossRefGoogle Scholar
  105. Tan K, Le Douarin NM (1991) Development of the nuclei and cell migration in the medulla oblongata. Application of the quail-chick chimera system. Anat Embryol 183:321–343.PubMedCrossRefGoogle Scholar
  106. Thoby-Brisson M, Trinh J-B, Champagnat J, Fortin G (2005) Emergence of the pre-Bötzinger respiratory rhythm generator in the mouse embryo. J Neurosci 25:4307–4318.PubMedCrossRefGoogle Scholar
  107. Thomas J-L, Spassky N, Perez Villegas EM et al (2000) Spatiotemporal development of oligodendrocytes in the embryonic brain. J Neurosci Res 59:471–476.PubMedCrossRefGoogle Scholar
  108. Torborg CL, Feller MB (2005) Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 76:213–235.PubMedCrossRefGoogle Scholar
  109. Tsau Y, Wenner P, O’Donovan MJ et al (1996) Dye screening and signal-to-noise ratio for retrogradely transported voltage-sensitive dyes. J Neurosci Methods 70:121–129.PubMedCrossRefGoogle Scholar
  110. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43:647–661.PubMedCrossRefGoogle Scholar
  111. Wenner P, O’Donovan MJ (2001) Mechanisms that initiate spontaneous network activity in the developing chick spinal cord. J Neurophysiol 86:1481–1498.PubMedGoogle Scholar
  112. Wenner P, Tsau Y, Cohen LB, O’Donovan MJ, Dan Y (1996) Voltage-sensitive dye recording using retrogradely transported dye in the chicken spinal cord: staining and signal characteristics. J Neurosci Methods 70:111–120.PubMedCrossRefGoogle Scholar
  113. Wong ROL (1999) Retinal waves and visual system development. Ann Rev Neurosci 22:29–47.PubMedCrossRefGoogle Scholar
  114. Wu J-Y, Cohen LB (1993) Fast multisite optical measurement of membrane potential. In: Mason WT (ed) Fluorescent and luminescent probes for biological activity. Academic Press, Boston, pp 389–404.Google Scholar
  115. Wu J-Y, Lam Y-W, Falk CX et al (1998) Voltage-sensitive dyes for monitoring multineuronal activity in the intact central nervous system. Histochem J 30:169–187.PubMedCrossRefGoogle Scholar
  116. Ziskind-Conhaim L, Redman S (2005) Spatiotemporal patterns of dorsal root-evoked network activity in the neonatal rat spinal cord: optical and intracellular recordings. J Neurophysiol 94:1952–1961.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Yoko Momose-Sato
    • 1
  • Katsushige Sato
    • 2
  • Kohtaro Kamino
    • 3
  1. 1.Department of Health and Nutrition, College of Human Environmental StudiesKanto Gakuin UniversityYokohamaJapan
  2. 2.Department of Health and Nutrition Sciences, Faculty of Human HealthKomazawa Women’s UniversityTokyoJapan
  3. 3.Tokyo Medical and Dental University/Chiba-Kashiwa Rehabilitation CollegeTokyoJapan

Personalised recommendations