Electrical coupling between locomotor-related excitatory interneurons in the mammalian spinal cord

Journal of Neuroscience

Volumn 26, Issue 33, 2006, Pages 8477-8483

  Hinckley, Christopher A ^a   Ziskind Conhaim, Lea ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Electrical coupling; Excitatory spinal interneurons; Gap junction mediated transmission; Locomotor related interneurons; Mouse spinal cord; Rhythm coordination

Indexed keywords

GREEN FLUORESCENT PROTEIN; HOMEOBOX PROTEIN 9; HOMEODOMAIN PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTRIC ACTIVITY; GAP JUNCTION; GENE CLUSTER; INTERNEURON; JUVENILE; LOCOMOTION; MAMMAL; MOUSE; NERVE EXCITABILITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REPORTER GENE; SPINAL CORD; SYNAPSE; TRANSGENIC MOUSE;

AGING; ANIMALS; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; INTERNEURONS; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; PERIODICITY; SPINAL CORD; SYNAPSES; TRANSCRIPTION FACTORS;

EID: 33748133840     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0395-06.2006     Document Type: Article

References (44)

1. Arber S, Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S (1999) Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23:659-674.
2. Bennett MVL (1997) Electrical transmission: a functional analysis and comparison with chemical transmission. In: Cellular biology of neurons, handbook of physiology, the nervous system, Vol 1 (Kandel ER, ed), pp 357-416. Baltimore: Williams and Wilkins.
3. Chang Q, Balice-Gordon RJ (2000) Gap junctional communication among developing and injured motor neurons. Brain Res Brain Res Rev 32:242-249.
4. Chang Q, Gonzalez M, Pinter MJ, Balice-Gordon RJ (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J Neurosci 19:10813-10828.
5. Connors BW, Long MA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393-418.
6. Dermietzel R, Spray DC (1993) Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 16:186-192.
7. Devor A, Yarom Y (2002) Electrotonic coupling in the inferior olivary nucleus revealed by simultaneous double patch recordings. J Neurophysiol 87:3048-3058.
8. Draguhn A, Traub RD, Achmitz D, Jefferys JG (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189-192.
9. Fulton BP, Miledi R, Takahashi T (1980) Electrical synapses between motoneurons in the spinal cord of the newborn rat. Proc R Soc Lond B Biol Sci 208:115-120.
10. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
11. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2:425-433.
12. Gao BX, Stricker C, Ziskind-Conhaim L (2001) Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J Neurophysiol 86:492-502.
13. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
14. Gibson JR, Beierlein M, Connors BW (2005) Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J Neurophysiol 93:467-480.
15. Glover JC, Petursdottir G, Jansen JK (1986) Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo. J Neurosci Methods 18:243-254.
16. Hinckley C, Seebach B, Ziskind-Conhaim L (2005a) Distinct roles of glycinergic and GABAergic inhibition in coordinating locomotor-like rhythms in the neonatal mouse spinal cord. Neuroscience 131:745-758.
17. Hinckley CA, Hartley R, Wu L, Todd A, Ziskind-Conhaim L (2005b) Locomotor-like rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. J Neurophysiol 93:1439-1449.
18. Hornstein EP, Verweij J, Schnapf JL (2004) Electrical coupling between red and green cones in primate retina. Nat Neurosci 7:745-750.
19. Kandler K, Katz LC (1995) Neuronal coupling and uncoupling in the developing nervous system. Curr Opin Neurobiol 5:98-105.
20. Kiehn O, Tresch MC (2002) Gap junctions and motor behavior. Trends Neurosci 25:108-115.
21. Lin JY, van Wyk M, Bowala TK, Teo M-Y, Lipski J (2003) Dendritic projections and dye-coupling in dopaminergic neurons of the substantia nigra examined in horizontal brain slices from young rats. J Neurophysiol 90:2531-2535.
22. Llinas R, Yarom Y (1986) Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study. J Physiol (Lond) 376:163-182.
23. Logan SD, Pickering AE, Gibson IC, Nolan MF, Spanswick D (1996) Electrotonic coupling between rat sympathetic preganglionic neurones in vitro. J Physiol (Lond) 495:491-502.
24. MacVicar BA, Dudek FE (1981) Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213:782-785.
25. Mann-Metzer P, Yarom Y (1999) Electronic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J Neurosci 19:3298-3306.
26. Marder E (1998) Electrical synapses: beyond speed and synchrony to computation. Curr Biol 8:R795-R797.
27. Milner LD, Landmesser LT (1999) Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J Neurosci 19:3007-3022.
28. Neyton J, Trautmann A (1985) Single-channel currents of an intercellular junction. Nature 317:331-335.
29. Nolan MF, Logan SD, Spanswick D (1999) Electrophysiological properties of electrical synapses between rat sympathetic preganglionic neurones in vitro. J Physiol (Lond) 519:753-764.
30. Norekian TP (1999) GABAergic excitatory synapses and electrical coupling sustain prolonged discharges in the prey capture neural network of Clione limacina. J Neurosci 19:1863-1875.
31. Pastor AM, Mentis GZ, De La Cruz RR, Diaz E, Navarrete R (2003) Increased electrotonic coupling in spinal motoneurons after transient botulinum neurotoxin paralysis in the neonatal rat. J Neurophysiol 89:793-805.
32. Rekling JC, Feldman JL (1997) Bidirectional electrical coupling between inspiratory motoneurons in the newborn mouse nucleus ambiguus. J Neurophysiol 78:3508-3510.
33. Rekling JC, Shao XM, Feldman JL (2000) Electrical coupling and excitatory synaptic transmission between rhythmogenic respiratory neurons in the preBotzinger complex. J Neurosci 20:RC113(1-5).
34. Saint-Amant L, Drapeau P (2001) Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 31:1035-1046.
35. Seebach BS, Ziskind-Conhaim L (1994) Formation of transient inappropriate sensorimotor synapses in developing rat spinal cords. J Neurosci 14:4520-4528.
36. Teubner B, Degen J, Söhl G, Güldenagel M, Bukauskas FF, Trexler EB, Verselis VK, De Zeeuw CI, Lee CG, Kozak CA, Petrasch-Parwez E, Dermietzel R, Willecke K (2000) Functional expression of the murine connexin 36 gene coding for a neuron-specific gap junctional protein. J Membr Biol 176:249-262.
37. Thaler J, Harrison K, Sharma K, Lettieri K, Kehrl J, Pfaff SL (1999) Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23:675-687.
38. Tresch MC, Kiehn O (2000) Motor coordination without action potentials in the mammalian spinal cord. Nat Neurosci 3:593-599.
39. Walton KD, Navarrete R (1991) Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. J Physiol (Lond) 433:283-305.
40. Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397.
41. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM (2005) Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25:5710-5719.
42. Ziskind-Conhaim L (1990) NMDA receptors mediate poly- and monosynaptic potentials in motoneurons of rat embryos. J Neurosci 10:125-135.
43. Ziskind-Conhaim L, Hinckley CA (2005) Electrical coupling between rhythmic HB9-expressing interneurons in the mammalian spinal cord. Soc Neurosci Abstr 31:516.11.
44. Ziskind-Conhaim L, Gao BX, Hinckley C (2003) Ethanol dual modulatory actions on spontaneous postsynaptic currents in spinal motoneurons. J Neurophysiol 89:806-813.