A subcortical inhibitory signal for behavioral arrest in the thalamus

Nature Neuroscience

Volumn 18, Issue 4, 2015, Pages 562-568

  Giber, Kristóf ^a   Diana, Marco A ^b,c,d   M Plattner, Viktor ^a   Dugué, Guillaume P ^b,c,d   Bokor, Hajnalka ^a   Rousseau, Charly V ^b,c,d   Maglóczky, Zsófia ^a   Havas, László ^e   Hangya, Balázs ^a,f   Wildner, Hendrik ^g   Zeilhofer, Hanns Ulrich ^g,h   Dieudonné, Stéphane ^b,c,d   Acsády, László ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b PSL RESEARCH UNIVERSITY   (France)

^c INSERM   (France)

^d CNRS   (France)

^e St Borbala Hospital   (Hungary)

^f Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^g UNIVERSITY OF ZURICH   (Switzerland)

^h ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FEMALE; GABAERGIC SYSTEM; GENE ACTIVATION; HUMAN; HUMAN TISSUE; MALE; MOUSE; MOVEMENT (PHYSIOLOGY); NERVE FIBER; NONHUMAN; OPTOGENETICS; OSCILLATION; PHENOTYPE; PONS RETICULAR FORMATION; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC INHIBITION; THALAMUS; WAKEFULNESS; ANIMAL; ANIMAL BEHAVIOR; METABOLISM; NERVE CELL INHIBITION; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PONTINE TEGMENTUM; SENSORY NERVE; THALAMUS INTRALAMINAR NUCLEUS;

4 AMINOBUTYRIC ACID RECEPTOR; GLYCINE; GLYCINE RECEPTOR;

AFFERENT PATHWAYS; ANIMALS; BEHAVIOR, ANIMAL; GABAERGIC NEURONS; GLYCINE; INTRALAMINAR THALAMIC NUCLEI; MALE; MICE; NERVE FIBERS; NEURAL INHIBITION; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; PONTINE TEGMENTUM; RECEPTORS, GABA; RECEPTORS, GLYCINE;

EID: 84925768132     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3951     Document Type: Article

References (47)

1. Drew, T., Andujar, J.-E., Lajoie, K. & Yakovenko, S. Cortical mechanisms involved in visuomotor coordination during precision walking. Brain Res. Rev. 57, 199-211 (2008).
2. Lemon, R.N. Descending pathways in motor control. Annu. Rev. Neurosci. 31, 195-218 (2008).
3. Rizzolatti, G. & Luppino, G. The cortical motor system. Neuron 31, 889-901 (2001).
4. Graybiel, A.M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31, 359-387 (2008).
5. Isoda, M. & Hikosaka, O. Cortico-basal ganglia mechanisms for overcoming innate, habitual and motivational behaviors. Eur. J. Neurosci. 33, 2058-2069 (2011).
6. Marder, E. & Calabrese, R.L. Principles of rhythmic motor pattern generation. Physiol. Rev. 76, 687-717 (1996).
7. Rossignol, S., Dubuc, R. & Gossard, J.-P. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86, 89-154 (2006).
8. Hajnik, T., Lai, Y.Y. & Siegel, J.M. Atonia-related regions in the rodent pons and medulla. J. Neurophysiol. 84, 1942-1948 (2000).
9. Klemm, W.R. Behavioral arrest: in search of the neural control system. Prog. Neurobiol. 65, 453-471 (2001).
10. Buzsaki, G. Rhythms of the Brain (Oxford University Press, 2006).
11. Cabral, J., Kringelbach, M.L. & Deco, G. Exploring the network dynamics underlying brain activity during rest. Prog. Neurobiol. 114, 102-131 (2014).
12. Krout, K.E., Belzer, R.E. & Loewy, A.D. Brainstem projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol. 448, 53-101 (2002).
13. Groenewegen, H.J. & Berendse, H.W. The specifcity of the "nonspecifc" midline and intralaminar thalamic nuclei. Trends Neurosci. 17, 52-57 (1994).
14. Bogen, J.E. On the neurophysiology of consciousness. I. An overview. Conscious. Cogn. 4, 52-62 (1995).
15. Kinney, H.C., Korein, J., Panigrahy, A., Dikkes, P. & Goode, R. Neuropathological fndings in the brain of Karen Ann Quinlan: the role of the thalamus in the persistent vegetative state. N. Engl. J. Med. 330, 1469-1475 (1994).
16. Schiff, N.D., Giacino, J., Kalmar, K. & Victor, J. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600-603 (2007).
17. Zeilhofer, H.U. et al. Glycinergic neurons expressing enhanced green fuorescent protein in bacterial artifcial chromosome transgenic mice. J. Comp. Neurol. 482, 123-141 (2005).
18. Yeo, S.S., Chang, P.H. & Jang, S.H. The ascending reticular activating system from pontine reticular formation to the thalamus in the human brain. Front. Hum. Neurosci. 7, 416 (2013).
19. Edlow, B.L. et al. Neuroanatomic connectivity of the human ascending arousal system critical to consciousness and its disorders. J. Neuropathol. Exp. Neurol. 71, 531-546 (2012).
20. Jones, E.G. The Thalamus (Cambridge University Press, 2007).
21. Wanaverbecq, N. et al. Contrasting the functional properties of GABAergic axon terminals with single and multiple synapses in the thalamus. J. Neurosci. 28, 11848-11861 (2008).
22. Telgkamp, P., Padgett, D.E., Ledoux, V.A., Woolley, C.S. & Raman, I.M. Maintenance of high-frequency transmission at Purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron 41, 113-126 (2004).
23. Todd, A.J. GABA and glycine in synaptic glomeruli of the rat spinal dorsal horn. Eur. J. Neurosci. 8, 2492-2498 (1996).
24. Russier, M., Kopysova, I.L., Ankri, N., Ferrand, N. & Debanne, D. GABA and glycine co-release optimizes functional inhibition in rat brainstem motoneurons in vitro. J. Physiol. (Lond.) 541, 123-137 (2002).
25. Chauvette, S., Crochet, S., Volgushev, M. & Timofeev, I. Properties of slow oscillation during slow-wave sleep and anesthesia in cats. J. Neurosci. 31, 14998-15008 (2011).
26. Parvizi, J. & Damasio, A.R. Neuroanatomical correlates of brainstem coma. Brain 126, 1524-1536 (2003).
27. Bokor, H. et al. Selective GABAergic control of higher-order thalamic relays. Neuron 45, 929-940 (2005).
28. Lu, J. et al. Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron 55, 874-889 (2007).
29. Dugué, G.P., Dumoulin, A., Triller, A. & Dieudonné, S. Target-dependent use of co-released inhibitory transmitters at central synapses. J. Neurosci. 25, 6490-6498 (2005).
30. Rousseau, C.V. et al. Mixed inhibitory synaptic balance correlates with glutamatergic synaptic phenotype in cerebellar unipolar brush cells. J. Neurosci. 32, 4632-4644 (2012).
31. Elazar, Z. & Paz, M. Catalepsy induced by carbachol microinjected into the pontine reticular formation of rats. Neurosci. Lett. 115, 226-230 (1990).
32. Brudzyński, S.M. & Mogenson, G.J. The role of the nucleus reticularis tegmenti pontis in locomotion: a lesion study in the rat. Brain Res. Bull. 12, 513-520 (1984).
33. Cheng, J.T., Schallert, T., De Ryck, M. & Teitelbaum, P. Galloping induced by pontine tegmentum damage in rats: a form of "Parkinsonian festination" not blocked by haloperidol. Proc. Natl. Acad. Sci. USA 78, 3279-3283 (1981).
34. Smith, Y. et al. The thalamostriatal system in normal and diseased states. Front. Syst. Neurosci. 8, 5 (2014).
35. Kravitz, A.V. et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466, 622-626 (2010).
36. Tecuapetla, F., Matias, S., Dugue, G.P., Mainen, Z.F. & Costa, R.M. Balanced activity in basal ganglia projection pathways is critical for contraversive movements. Nat. Commun. 5, 4315 (2014).
37. Doig, N.M., Moss, J. & Bolam, J.P. Cortical and thalamic innervation of direct and indirect pathway medium-sized spiny neurons in mouse striatum. J. Neurosci. 30, 14610-14618 (2010).
38. Leresche, N., Lightowler, S., Soltesz, I., Jassik-Gerschenfeld, D. & Crunelli, V. Low-frequency oscillatory activities intrinsic to rat and cat thalamocortical cells. J. Physiol. (Lond.) 441, 155-174 (1991).
39. Poulet, J.F.A. & Petersen, C.C.H. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881-885 (2008).
40. Ji, D. & Wilson, M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10, 100-107 (2007).
41. Vyazovskiy, V.V. & Harris, K.D. Sleep and the single neuron: the role of global slow oscillations in individual cell rest. Nat. Rev. Neurosci. 14, 443-451 (2013).
42. Ollion, J., Cochennec, J., Loll, F., Escudé, C. & Boudier, T. TANGO: a generic tool for high-throughput 3D image analysis for studying nuclear organization. Bioinformatics 29, 1840-1841 (2013).
43. Somogyi, P., Hodgson, A.J., Chubb, I.W., Penke, B. & Erdei, A. Antisera to gamma-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J. Histochem. Cytochem. 33, 240-248 (1985).
44. Pinault, D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J. Neurosci. Methods 65, 113-136 (1996).
45. Slézia, A., Hangya, B., Ulbert, I. & Acsády, L. Phase advancement and nucleus-specifc timing of thalamocortical activity during slow cortical oscillation. J. Neurosci. 31, 607-617 (2011).
46. Hurtado, J.M., Rubchinsky, L.L. & Sigvardt, K.A. Statistical method for detection of phase-locking episodes in neural oscillations. J. Neurophysiol. 91, 1883-1898 (2004).
47. Fisher, N. Statistical Analysis of Circular Data (Cambridge University Press, 1993).