Regulation of interneuron excitability by gap junction coupling with principal cells

Nature Neuroscience

Volumn 16, Issue 12, 2013, Pages 1764-1772

  Apostolides, Pierre F ^a   Trussell, Laurence O ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 36;

ACOUSTIC NERVE FIBER; ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL STRUCTURE; COCHLEAR NERVE; DORSAL COCHLEAR NUCLEUS; ELECTRICAL SYNAPSE; ELECTROPHYSIOLOGY; GAP JUNCTION; HYPERPOLARIZATION; INTERNEURON; INTRACELLULAR RECORDING; MEMBRANE POTENTIAL; MOUSE; NERVE CELL EXCITABILITY; NERVE CONDUCTION; NONHUMAN; OPTOGENETICS; PATCH CLAMP; PRIORITY JOURNAL; SPINDLE CELL; STELLATE CELL;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICAL PHENOMENA; COCHLEAR NUCLEUS; CONNEXINS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GAP JUNCTIONS; INTERNEURONS; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE NET; NEURAL INHIBITION; NEURONS; NEUROTRANSMITTER AGENTS; RHODOPSIN; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84888330573     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3569     Document Type: Article

References (47)

1. Bell, C.C., Han, V. & Sawtell, N.B. Cerebellum-like structures and their implications for cerebellar function. Annu. Rev. Neurosci. 31, 1-24 (2008
2. Dean, P., Porrill, J., Ekerot, C-F. & Jörntell, H. The cerebellar microcircuit as an adaptive filter: Experimental and computational evidence. Nat. Rev. Neurosci. 11, 30-43 (2010
3. Requarth, T. & Sawtell, N.B. Neural mechanisms for filtering self-generated sensory signals in cerebellum-like circuits. Curr. Opin. Neurobiol. 21, 602-608 (2011
4. Oertel, D. & Young, E.D. What's a cerebellar circuit doing in the auditory system? Trends Neurosci. 27, 104-110 (2004
5. Roberts, M.T. & Trussell, L.O. Molecular layer inhibitory interneurons provide feedforward and lateral inhibition in the dorsal cochlear nucleus. J. Neurophysiol. 104, 2462-2473 (2010
6. Bennett, M.V.L. & Zukin, R.S. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41, 495-511 (2004
7. Hestrin, S. & Galarreta, M. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci. 28, 304-309 (2005
8. Christie, M.J., Williams, J.T. & North, R.A. Electrical coupling synchronizes subthreshold activity in locus coeruleus neurons in vitro from neonatal rats. J. Neurosci. 9, 3584-3589 (1989
9. Maher, B.J., McGinley, M.J. & Westbrook, G.L. Experience-dependent maturation of the glomerular microcircuit. Proc. Natl. Acad. Sci. USA 106, 16865-16870 (2009
10. Bennett, M.V. Physiology of electrotonic junctions. Ann. NY Acad. Sci. 137, 509-539 (1966
11. Gibson, J.R., Beierlein, M. & Connors, B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79 (1999
12. Wouterlood, F.G., Mugnaini, E., Osen, K.K. & Dahl, A.L. Stellate neurons in rat dorsal cochlear nucleus studies with combined Golgi impregnation and electron microscopy: Synaptic connections and mutual coupling by gap junctions. J. Neurocytol. 13, 639-664 (1984
13. Mann-Metzer, P. & Yarom, Y. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J. Neurosci. 19, 3298-3306 (1999
14. Leao, R.M., Li, S., Doiron, B. & Tzounopoulos, T. Diverse levels of an inwardly rectifying potassium conductance generate heterogeneous neuronal behavior in a population of dorsal cochlear nucleus pyramidal neurons. J. Neurophysiol. 107, 3008-3019 (2012
15. Davis, K.A. & Young, E.D. Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J. Neurophysiol. 83, 926-940 (2000
16. Molitor, S.C. & Manis, P.B. Dendritic Ca2+ transients evoked by action potentials in rat dorsal cochlear nucleus pyramidal and cartwheel neurons. J. Neurophysiol. 89, 2225-2237 (2003
17. Tzounopoulos, T., Kim, Y., Oertel, D. & Trussell, L.O. Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat. Neurosci. 7, 719-725 (2004
18. Zhang, S. & Oertel, D. Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. J. Neurophysiol. 71, 914-930 (1994
19. Dugué, G.P. et al. Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network. Neuron 61, 126-139 (2009
20. Vervaeke, K. et al. Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron 67, 435-451 (2010
21. Gibson, J.R., Beierlein, M. & Connors, B.W. Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J. Neurophysiol. 93, 467-480 (2005
22. Ma, W-L.D. & Brenowitz, S.D. Single-neuron recordings from unanesthetized mouse dorsal cochlear nucleus. J. Neurophysiol. 107, 824-835 (2012
23. Rhode, W.S., Smith, P.H. & Oertel, D. Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. J. Comp. Neurol. 213, 426-447 (1983
24. Hancock, K.E. & Voigt, H.F. Intracellularly labeled fusiform cells in dorsal cochlear nucleus of the gerbil. I. Physiological response properties. J. Neurophysiol. 87, 2505-2519 (2002
25. Merchan, M.A., Collia, F.P., Merchan, J.A. & Saldana, E. Distribution of primary afferent fibres in the cochlear nuclei. A silver and horseradish peroxidase (HRP) study. J. Anat. 141, 121-130 (1985
26. Arenkiel, B.R. et al. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54, 205-218 (2007
27. Hägglund, M., Borgius, L., Dougherty, K.J. & Kiehn, O. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat. Neurosci. 13, 246-252 (2010
28. Ito, T. & Oliver, D.L. Origins of glutamatergic terminals in the inferior colliculus identified by retrograde transport and expression of VGLUT1 and VGLUT2 genes. Front. Neuroanat. 4, 135 (2010
29. Mugnaini, E. GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: Light and electron microscopic immunocytochemistry. J. Comp. Neurol. 235, 61-81 (1985
30. Nagel, G. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100, 13940-13945 (2003
31. Mitchell, S.J. & Silver, R.A. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433-445 (2003
32. Rubio, M.E. & Juiz, J.M. Differential distribution of synaptic endings containing glutamate, glycine, and GABA in the rat dorsal cochlear nucleus. J. Comp. Neurol. 477, 253-272 (2004); erratum 485, 266 (2005
33. Isaacson, J.S. & Scanziani, M. How inhibition shapes cortical activity. Neuron 72, 231-243 (2011
34. Osen, K.K., Ottersen, O.P. & Storm-Mathisen, J. Colocalization of glycine-like and GABA-like immunoreactivities: A semi-quantitative study of individual neurons in the dorsal cochlear nucleus of cat. in Glycine Neurotransmission (eds. Ottersen, O.P. & Storm-Mathisen, J.): 417-451 (J. Wiley and Sons, New York, 1990
35. Bell, C.C., Han, V.Z., Sugawara, Y. & Grant, K. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387, 278-281 (1997
36. Han, V.Z., Grant, K. & Bell, C.C. Reversible associative depression and nonassociative potentiation at a parallel fiber synapse. Neuron 27, 611-622 (2000
37. Bell, C.C., Caputi, A. & Grant, K. Physiology and plasticity of morphologically identified cells in the mormyrid electrosensory lobe. J. Neurosci. 17, 6409-6423 (1997
38. Sawtell, N.B. & Williams, A. Transformations of electrosensory encoding associated with an adaptive filter. J. Neurosci. 28, 1598-1612 (2008
39. Hansel, C. et al. αCaMKII Is essential for cerebellar LTD and motor learning. Neuron 51, 835-843 (2006
40. Szapiro, G. & Barbour, B. Multiple climbing fibers signal to molecular layer interneurons exclusively via glutamate spillover. Nat. Neurosci. 10, 735-742 (2007
41. Mathews, P.J., Lee, K.H., Peng, Z., Houser, C.R. & Otis, T.S. Effects of climbing fiber driven inhibition on Purkinje neuron spiking. J. Neurosci. 32, 17988-17997 (2012
42. Coddington, L.T., Rudolph, S., Vande Lune, P., Overstreet-Wadiche, L. & Wadiche, J.I. Spillover-mediated feedforward inhibition functionally segregates interneuron activity. Neuron 78, 1050-1062 (2013
43. Zhao, S. et al. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat. Methods 8, 745-752 (2011
44. Kuo, S.P. & Trussell, L.O. Spontaneous spiking and synaptic depression underlie noradrenergic control of feed-forward inhibition. Neuron 71, 306-318 (2011
45. Apostolides, P.F. & Trussell, L.O. Rapid, Activity-independent turnover of vesicular transmitter content at a mixed glycine/GABA synapse. J. Neurosci. 33, 4768-4781 (2013
46. Bender, K.J., Ford, C.P. & Trussell, L.O. Dopaminergic modulation of axon initial segment calcium channels regulates action potential initiation. Neuron 68, 500-511 (2010
47. Devor, A. & Yarom, Y. Electrotonic coupling in the inferior olivary nucleus revealed by simultaneous double patch recordings. J. Neurophysiol. 87, 3048-3058 (2002