Sequential development of electrical and chemical synaptic connections generates a specific behavioral circuit in the leech

Journal of Neuroscience

Volumn 25, Issue 10, 2005, Pages 2478-2489

  Marin Burgin, Antonia ^a   Eisenhart, F James ^a,b   Baca, Serapio M ^a   Kristan Jr , William B ^a   French, Kathleen A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MICROSOFT   (United States)

Author keywords

Behavior; Development; Gap junction; Imaging; Invertebrate; Synapse

Indexed keywords

BICUCULLINE METHIODIDE;

ARTICLE; BEHAVIOR; DEVELOPMENT; ELECTROPHYSIOLOGY; EMBRYO DEVELOPMENT; GABAERGIC TRANSMISSION; INTERNEURON; LEECH; MOTONEURON; MOVEMENT (PHYSIOLOGY); NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; STATISTICS; SYNAPSE;

ANIMALS; BEHAVIOR, ANIMAL; ELECTRICITY; HIRUDO MEDICINALIS; NERVE NET; PHYSICAL STIMULATION; SYNAPSES;

EID: 14944368281     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4787-04.2005     Document Type: Article

References (70)

1. Bate M (1999) Development of motor behaviour. Curr Opin Neurobiol 9:670-675.
2. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
3. Bennett MV (1966) Physiology of electro tonic junctions. Ann NY Acad Sci 137:509-539.
4. Bennett MVL (2000a) Electrical synapses, a personal perspective (or history). Brain Res Rev 32:16-28.
5. Bennett MVL (2000b) Seeing is relieving: electrical synapses between visualized neurons. Nat Neurosci 3:7-9.
6. Blagburn JM, Sosa MA, Blanco RE (1996) Specificity of identified central synapses in the embryonic cockroach - appropriate connections form before the onset of spontaneous afferent activity 373:511-528.
7. Bonnot AS, Whelan PJ, Mentis GZ, O'Donovan MJ (2002) Spatiotemporal pattern of motoneuron activation in the rostral lumbar and the sacral segments during locomotor-like activity in the neonatal mouse spinal cord. J Neurosci 22:RC203(1-6).
8. Borrell V, Callaway EM (2002) Reorganization of exuberant axonal arbors contributes to the development of laminar specificity in ferret visual cortex. J Neurosci 22:6682-6695.
9. Brocard F, Vinay L, Clarac F (1999) Development of hindlimb postural control during the first postnatal week in the rat. Dev Brain Res 117:81-89.
10. Bureau I, Shepherd GMG, Svoboda K (2004) Precise development of functional and anatomical columns in the neocortex. Neuron 42:789-801.
11. Cacciatore TW, Brodfuehrer PD, Gonzalez JE, Jiang T, Adams SR, Tsien RY, Kristan WB, Kleinfeld D (1999) Identification of neural circuits by imaging coherent electrical activity with FRET-based dyes. Neuron 23:449-459.
12. Cazalets JR, Borde M, Clarac F (1996) The synaptic drive from the spinal locomotor network to motoneurons in the newborn rat. J Neurosci 16:298-306.
13. Chang Q, Gonzalez M, Pinter MJ, Balice-Gordon RJ (1999) Gap functional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J Neurosci 19:10813-10828.
14. Chiba A, Murphey RK (1991) Connectivity of identified central synapses in the cricket is normal following regeneration and blockade of presynaptic activity. J Neurobiol 22:130-142.
15. Chiba A, Shepherd D, Murphey RK (1988) Synaptic rearrangement during postembryonic development in the cricket 240:901-905.
16. Cline HT (1983) Tritium labeled gamma amino butyric-acid uptake selectively labels identifiable neurons in the leech central nervous system. J Comp Physiol 215:351-358.
17. Cline HT (1986) Evidence for GABA as a neurotransmitter in the leech. J Neurosci 6:2848-2856.
18. Crespel F, Mariani J, Delhaye-Bouchaud N (1976) Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J Neurobiol 7:567-578.
19. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL (2001) Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing Connexin36. Neuron 31:477-485.
20. Debski EA, Cline HT (2002) Activity-dependent mapping in the retinotectal projection. Curr Opin Neurobiol 12:93-99.
21. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Brustein E (2002) Development of the locomotor network in zebrafish. Prog Neurobiol 68:85-111.
22. Dykes IM, Freeman FM, Bacon JP, Davies JA (2004) Molecular basis of gap junctional communication in the CNS of the leech Hirudo medicinalis. J Neurosci 24:886-894.
23. Easter Jr SS, Purves D, Rakic P, Spitzer NC (1985) The changing view of neural specificity. Science 230:507-511.
24. Eisenhart FJ, Kristan Jr WB (1999) A quantitative analysis of neurobiotin coupling demonstrates that leech neurons form transient electrical synapses during development. Soc Neurosci Abstr 25:202.11.
25. Fischbach GD (1972) Synapse formation between dissociated nerve and muscle cells in low density cell cultures. Dev Biol 28:407-429.
26. Galarreta W, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
27. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
28. Glover JC (2000) Development of specific connectivity between premotor neurons and motoneurons in the brain stem and spinal cord. Physiol Rev 80:615-647.
29. Gonzalez JE, Tsien RY (1995) Voltage sensing by fluorescence resonance energy transfer in single cells. Biophys J 69:1272-1280.
30. Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72:77-98.
31. Granzow B, Kristan Jr WB (1986) Inhibitory connections between motor neurons modify a centrally generated motor pattern in the leech nervous system. Brain Res 369:321-325.
32. Granzow B, Friesen W, Kristan Jr WB (1985) Physiological and morphological analysis of synaptic transmission between leech motor neurons. J Neurosci 8:2035-2050.
33. Jacobs G, Weeks J (1990) Postsynaptic changes at a sensory-to-motoneuron synapse contribute to the developmental loss of a reflex behavior during insect metamorphosis. J Neurosci 10:1341-1356.
34. Kandler K, Katz LC (1995) Neuronal coupling and uncoupling in the developing nervous system. Curr Opin Neurobiol 5:98-105.
35. Katz LC (1991) Specificity in the development of vertical connections in cat striate cortex. Eur J Neurosci 3:1-10.
36. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
37. Kristan Jr WB (1982) Sensory and motor neurons responsible for the local bending response in leeches. J Exp Biol 96:161-180.
38. Kristan Jr WB, Eisenhart FJ, Johnson LA, French KA (2000) Development of neuronal circuits and behaviors in the medicinal leech. Brain Res Bull 53:561-570.
39. Levine RB, Truman JW (1982) Metamorphosis of the insect nervous system changes in morphology and synaptic interactions of identified neurons. Nature 299:250-252.
40. Lewis JE, Kristan Jr WB (1998) A neuronal network for computing population vectors in the leech. Nature 391:76-79.
41. Lichtman JW, Colman H (2000) Synapse elimination and indelible memory. Neuron 25:269-278.
42. Lockery SR, Kristan Jr WB (1990) Distributed processing of sensory information in the leech. II. Identification of interneurons contributing to the local bending reflex. J Neurosci 10:1816-1829.
43. Long MA, Landisman CE, Connors BW (2004) Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J Neurosci 24:341-349.
44. Lucas BD, Kanade T (1981) An iterative image registration technique with an application to stereo vision (IJCAI). In: Proceedings of the 7th International Joint Conference on Artificial Intelligence, pp 674-679. San Francisco: Morgan Kaufmann.
45. Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687-717.
46. Muller KJ, Nicholls JG, Stent GS (1981) Neurobiology of the leech. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
47. Nakayama K, Nishimaru H, Kudo N (2002) Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22:10388-10398.
48. Nishimaru H, Kudo N (2000) Formation of the central pattern generator for locomotion in the rat and mouse. Brain Res Bull 53:661-669.
49. O'Donovan M, Sernagor E, Sholomenko G, Ho S, Antal M, Yee W (1992) Development of spinal motor networks in the chick embryo. J Exp Zool 261:261-273.
50. Ort CA, Kristan Jr WB, Stent GS (1974) Neuronal control of swimming in the medicinal leech. II. Identification and connections of motor neurons. J Comp Physiol 94:121-154.
51. Peinado A, Yuste R, Katz LC (1993a) Gap junctional communication and the development of local circuits in neocortex. Cereb Cortex 3:488-498.
52. Peinado A, Yuste R, Katz LC (1993b) Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10:103-114.
53. Penn AA, Wong ROL, Shatz CJ (1994) Neuronal coupling in the developing mammalian retina. J Neurosci 14:3805-3815.
54. Purves D, Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210:153-157.
55. Reynolds SA, French KA, Baader A, Kristan Jr WB (1998a) Staging of middle and late embryonic development in the medicinal leech, Hirudo medicinalis. J Comp Neurol 402:155-167.
56. Reynolds SA, French KA, Baader A, Kristan Jr WB (1998b) Development of spontaneous and evoked behaviors in the medicinal leech. J Comp Neurol 402:168-180.
57. Rink TJ, Tsien RY, Warner AE (1980) Free calcium in Xenopus laevis embryos measured with ion selective microelectrodes. Nature 283:658-660.
58. Roerig B, Feller MB (2000) Neurotransmitters and gap junctions in developing neural circuits. Brain Res Rev 32:86-114.
59. Ruthazer ES, Akerman CJ, Cline HT (2003) Control of axon branch dynamics by correlated activity in vivo. Science 301:66-70.
60. Sawada M, Wilkinson JM, McAdoo DJ, Coggeshall RE (1976) The identification of 2 inhibitory cells in each segmental ganglion of the leech and studies on the ionic mechanism of the inhibitory junctional potentials produced by these cells. J Neurobiol 7:435-445.
61. Shepherd D, Murphey RK (1986) Competition regulates the efficacy of an identified synapse in crickets. J Neurosci 6:3152-3160.
62. Sillar KT, Simmers AJ (1994) Electrical coupling and intrinsic neuronal oscillations in rana temporaria spinal cord. Eur J Morphol 32:293-298.
63. Stuart AE (1970) Physiological and morphological properties of motoneurones in the central nervous system of the leech. J Physiol (Lond) 209:627-646.
64. Szabo TM, Faber DS, Zoran MJ (2004) Transient electrical coupling delays the onset of chemical neurotransmission at developing synapses. J Neurosci 24:112-120.
65. Taylor AL, Cottrell GW, Kleinfeld D, Kristan Jr WB (2003) Imaging reveals synaptic targets of a swim-terminating neuron in the leech CNS. J Neurosci 23:11402-11410.
66. Tresch MC, Kiehn O (2000) Motor coordination without action potentials in the mammalian spinal cord. Nat Neurosci 3:593-599.
67. Tresch MC, Kiehn O (2002) Synchronization of motor neurons during locomotion in the neonatal rat: predictors and mechanisms. J Neurosci 22:9997-10008.
68. Walton KD, Navarrete R (1991) Postnatal changes in motoneuron electrotonic coupling studied in the in vitro rat lumbar spinal cord. J Physiol (Lond) 433:283-306.
69. Ye M, Haralick RM (2000) Image flow estimation using facet model and covariance propagation. In: Vision interface: real world applications of computer vision, Vol 35 (Cheriet M, Yang YH, eds), pp 209-241. Hackensack, NJ: World Scientific.
70. Zoccolan D, Torre V (2002) Using optical flow to characterize sensory-motor interactions in a segment of the medicinal leech. J Neurosci 22:2283-2298.