Decoding brain state transitions in the pedunculopontine nucleus: Cooperative phasic and tonic mechanisms

Frontiers in Neural Circuits

Volumn 9, Issue OCTOBER, 2015, Pages 1-16

  Petzold, Anne ^a,f   Valencia, Miguel ^b,c   Pál, Balázs ^d   Mena Segovia, Juan ^a,e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF NAVARRA   (Spain)

^c IdiSNA Navarra Institute for Health Research   (Spain)

^d UNIVERSITY OF DEBRECEN   (Hungary)

^e RUTGERS UNIVERSITY   (United States)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Arousal; Brainstem; Cholinergic neurons; Network activity; Oscillations; Phasic

Indexed keywords

ANIMAL EXPERIMENT; BRAIN; CHOLINERGIC NERVE CELL; CONFORMATIONAL TRANSITION; DRIVER; FIRING RATE; IN VITRO STUDY; NONHUMAN; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; SENSORY STIMULATION; ANIMAL; BRAIN CORTEX; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; MALE; NERVE CELL NETWORK; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN WAVES; CEREBRAL CORTEX; CHOLINERGIC NEURONS; ELECTROPHYSIOLOGICAL PHENOMENA; MALE; NERVE NET; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84948762042     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2015.00068     Document Type: Article

References (60)

1. Adamantidis, A. R., Zhang, F., Aravanis, A. M., Deisseroth, K., and de Lecea, L. (2007). Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420-424. doi: 10.1038/nature06310
2. Aston-Jones, G., and Bloom, F. E. (1981). Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle.J. Neurosci. 1, 876-886.
3. Barroso-Chinea, P., Rico, A. J., Conte-Perales, L., Gómez-Bautista, V., Luquin, N., Sierra, S., et al. (2011). Glutamatergic and cholinergic pedunculopontine neurons innervate the thalamic parafascicular nucleus in rats: changes following experimental parkinsonism. Brain Struct. Funct. 216, 319-330. doi: 10.1007/s00429-011-0317-x
4. Benjamini, Y., and Hocherg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B. 57, 289-300.
5. Blejec, A. (2005). Statistical method for detection of firing rate changes in spontaneously active neurons. Neurocomputing 65, 557-563. doi: 10.1016/j.neucom.2004.10.103
6. Boucetta, S., Cissé, Y., Mainville, L., Morales, M., and Jones, B. E. (2014). Discharge profiles across the sleep-waking cycle of identified cholinergic, GABAergic and glutamatergic neurons in the pontomesencephalic tegmentum of the rat. J. Neurosci.34, 4708-4727. doi: 10.1523/JNEUROSCI.2617-13.2014
7. Carter, M. E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., et al. (2010). Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 13, 1526-1533. doi: 10.1038/nn.2682
8. Clement, E. A., Richard, A., Thwaites, M., Ailon, J., Peters, S., and Dickson, C. T. (2008). Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS One 3:e2004. doi: 10.1371/journal.pone.0002004
9. Datta, S., Patterson, E. H., and Spoley, E. E. (2001). Excitation of the pedunculopontine tegmental NMDA receptors induces wakefulness and cortical activation in the rat. J. Neurosci. Res. 66, 109-116. doi: 10.1002/jnr.1202
10. Datta, S., and Siwek, D. F. (2002). Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats. J. Neurosci. Res. 70, 611-621. doi: 10.1002/jnr.10405
11. Dautan, D., Huerta-Ocampo, I., Witten, I. B., Deisseroth, K., Bolam, J. P., Gerdjikov, T., et al. (2014). A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J. Neurosci. 34, 4509-4518. doi: 10.1523/JNEUROSCI.5071-13.2014
12. Deurveilher, S., and Hennevin, E. (2001). Lesions of the pedunculopontine tegmental nucleus reduce paradoxical sleep (PS) propensity: evidence from a short-term PS deprivation study in rats. Eur. J. Neurosci. 13, 1963-1976. doi: 10.1046/j.0953-816x.2001.01562.x
13. Efron, B. (1979). Bootstrap methods: another look at the jackknife. Ann. Statist. 7, 1-26. doi: 10.1214/aos/1176344552
14. El Mansari, M., Sakai, K., and Jouvet, M. (1989). Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp. Brain Res. 76, 519-529. doi: 10.1007/bf00248908
15. Fisher, N. I. (1993). Statistical Analysis of Circular Data. Cambridge: Cambridge University Press.
16. Fornal, C., Auerbach, S., and Jacobs, B. L. (1985). Activity of serotonin-containing neurons in nucleus raphe magnus in freely moving cats. Exp. Neurol. 88, 590-608. doi: 10.1016/0014-4886(85)90074-3
17. Gama, R. L., Távora, D. G., Bomfim, R. C., Silva, C. E., de Bruin, V. M., and de Bruin, P. F. (2010). Sleep disturbances and brain MRI morphometry in Parkinson's disease, multiple system atrophy and progressive supranuclear palsy - a comparative study.Parkinsonism Relat. Disord. 16, 275-279. doi: 10.1016/j.parkreldis.2010.01.002
18. Gonon, F., and Sundstrom, L. (1996). Excitatory effects of dopamine released by impulse flow in the rat nucleus accumbens in vivo. Neuroscience 75, 13-18. doi: 10.1016/0306-4522(96)00320-x
19. Halliday, D. M., Rosenberg, J. R., Amjad, A. M., Breeze, P., Conway, B. A., and Farmer, S. F. (1995). A framework for the analysis of mixed time series/point process data-theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog. Biophys. Mol. Biol. 64, 237-278. doi: 10.1016/s0079-6107(96)00009-0
20. Hong, S., and Hikosaka, O. (2014). Pedunculopontine tegmental nucleus neurons provide reward, sensorimotor and alerting signals to midbrain dopamine neurons.Neuroscience 282, 139-155. doi: 10.1016/j.neuroscience.2014.07.002
21. Irmak, S. O., and de Lecea, L. (2014). Basal forebrain cholinergic modulation of sleep transitions. Sleep 37, 1941-1951. doi: 10.5665/sleep.4246
22. Ishibashi, M., Gumenchuk, I., Kang, B., Steger, C., Lynn, E., Molina, N. E., et al. (2015). Orexin receptor activation generates gamma band input to cholinergic and serotonergic arousal system neurons and drives an intrinsic Ca2+-dependent resonance in LDT and PPT cholinergic neurons. Front. Neurol. 6:120. doi: 10.3389/fneur.2015.00120
23. Lee, S. H., and Dan, Y. (2012). Neuromodulation of brain states. Neuron 76, 209-222. doi: 10.1016/j.neuron.2012.09.012
24. Lee, M. G., Hassani, O. K., and Jones, B. E. (2005). Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J. Neurosci. 25, 6716-6720. doi: 10.1523/jneurosci.1887-05.2005
25. MacLaren, D. A. A., Markovic, T., and Clark, S. D. (2014). Assessment of sensorimotor gating following selective lesions of cholinergic pedunculopontine neurons. Eur. J. Neurosci. 40, 3526-3537. doi: 10.1111/ejn.12716
26. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140. doi: 10.103538/nn.2467
27. Magill, P. J., Pogosyan, A., Sharott, A., Csicsvari, J., Bolam, J. P., and Brown, P. (2006). Changes in functional connectivity within the rat striatopallidal axis during global brain activation in vivo. J. Neurosci. 26, 6318-6329. doi: 10.1523/jneurosci.0620-06.2006
28. Martinez-Gonzalez, C., Wang, H. L., Micklem, B. R., Bolam, J. P., and Mena-Segovia, J. (2012). Subpopulations of cholinergic, GABAergic and glutamatergic neurons in the pedunculopontine nucleus contain calcium-binding proteins and are heterogeneously distributed. Eur. J. Neurosci. 35, 723-734. doi: 10.1111/j.1460-9568.2012.08002.x
29. Mazère, J., Meissner, W. G., Mayo, W., Sibon, I., Lamare, F., Guilloteau, D., et al. (2012). Progressive supranuclear palsy: in vivo SPECT imaging of presynaptic vesicular acetylcholine transporter with [123I]-iodobenzovesamicol. Radiology 265, 537-543. doi: 10.1148/radiol.12112650
30. Mena-Segovia, J., Micklem, B. R., Nair-Roberts, R. G., Ungless, M. A., and Bolam, J. P. (2009). GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J. Comp. Neurol. 515, 397-408. doi: 10.1002/cne.22065
31. Mena-Segovia, J., Sims, H. M., Magill, P. J., and Bolam, J. P. (2008). Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J. Physiol. Lond. 586, 2947-2960. doi: 10.1113/jphysiol.2008.153874
32. Moruzzi, G., and Magoun, H. W. (1949). Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1, 455-473. doi: 10.1016/0013-4694(49)90219-9
33. Motelow, J. E., Li, W., Zhan, Q., Mishra, A. M., Sachdev, R. N., Liu, G., et al. (2015). Decreased subcortical cholinergic arousal in focal seizures. Neuron 85, 561-572. doi: 10.1016/j.neuron.2014.12.058
34. Nielsen, J. B., Conway, B. A., Halliday, D. M., Perreault, M. C., and Hultborn, H. (2005). Organization of common synaptic drive to motoneurones during fictive locomotion in the spinal cat. J. Physiol. 569, 291-304. doi: 10.1113/jphysiol.2005.091744
35. Nigro, M. J., Mateos-Aparicio, P., and Storm, J. F. (2014). Expression and functional roles of Kv7/KCNQ/M-channels in rat medial entorhinal cortex layer II stellate cells.J. Neurosci. 34, 6807-6812. doi: 10.1523/JNEUROSCI.4153-13.2014
36. Norton, A. B., Jo, Y. S., Clark, E. W., Taylor, C. A., and Mizumori, S. J. (2011). Independent neural coding of reward and movement by pedunculopontine tegmental nucleus neurons in freely navigating rats. Eur. J. Neurosci. 33, 1885-1896. doi: 10.1111/j.1460-9568.2011.07649.x
37. Okada, K., Toyama, K., Inoue, Y., Isa, T., and Kobayashi, Y. (2009). Different pedunculopontine tegmental neurons signal predicted and actual task rewards. J. Neurosci. 29, 4858-4870. doi: 10.1523/JNEUROSCI.4415-08.2009
38. Pan, W. X., and Hyland, B. I. (2005). Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J. Neurosci.25, 4725-4732. doi: 10.1523/jneurosci.0277-05.2005
39. Paré, D., Steriade, M., Deschênes, M., and Bouhassira, D. (1990). Prolonged enhancement of anterior thalamic synaptic responsiveness by stimulation of a brain-stem cholinergic group. J. Neurosci. 10, 20-33.
40. Paxinos, G., and Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates. 2nd Edn. San Diego: Academic Press.
41. Pinault, D. (1996). 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. doi: 10.1016/0165-0270(95)00144-1
42. Pincus, S. M. (1991). Approximate entropy as a measure of system complexity. Proc. Natl. Acad. Sci. U S A 88, 2297-2301. doi: 10.1073/pnas.88.6.2297
43. Ros, H., Magill, P. J., Moss, J., Bolam, J. P., and Mena-Segovia, J. (2010). Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states. Neuroscience 170, 78-91. doi: 10.1016/j.neuroscience.2010.06.068
44. Sakai, K. (2012). Discharge properties of presumed cholinergic and noncholinergic laterodorsal tegmental neurons related to cortical activation in non-anesthetized mice.Neuroscience 224, 172-190. doi: 10.1016/j.neuroscience.2012.08.032
45. Saper, C. B., Scammell, T. E., and Lu, J. (2005). Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257-1263. doi: 10.1038/nature04284
46. Sherin, J. E., Shiromani, P. J., McCarley, R. W., and Saper, C. B. (1996). Activation of ventrolateral preoptic neurons during sleep. Science 271, 216-219. doi: 10.1126/science.271.5246.216
47. Steininger, T. L., Alam, M. N., Gong, H., Szymusiak, R., and McGinty, D. (1999). Sleep-waking discharge of neurons in the posterior lateral hypothalamus of the albino rat.Brain Res. 840, 138-147. doi: 10.1016/s0006-8993(99)01648-0
48. Steriade, M. (2000). Corticothalamic resonance, states of vigilance and mentation.Neuroscience 101, 243-276. doi: 10.1016/s0306-4522(00)00353-5
49. Steriade, M. (2006). Grouping of brain rhythms in corticothalamic systems.Neuroscience 137, 1087-1106. doi: 10.1016/j.neuroscience.2005.10.029
50. Steriade, M., Datta, S., Paré, D., Oakson, G., and Curró Dossi, R. C. (1990). Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J. Neurosci. 10, 2541-2559.
51. Steriade, M., Dossi, R. C., Paré, D., and Oakson, G. (1991). Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proc. Natl. Acad. Sci. U S A 88, 4396-4400. doi: 10.1073/pnas.88.10.4396
52. Szymusiak, R., Alam, N., Steininger, T. L., and McGinty, D. (1998). Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats.Brain Res. 803, 178-188. doi: 10.1016/s0006-8993(98)00631-3
53. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., et al. (2011). A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron71, 995-1013. doi: 10.1016/j.neuron.2011.07.026
54. Thompson, J. A., and Felsen, G. (2013). Activity in mouse pedunculopontine tegmental nucleus reflects action and outcome in a decision-making task. J. Neurophysiol. 110, 2817-2829. doi: 10.1152/jn.00464.2013
55. Urbano, F. J., D'Onofrio, S. M., Luster, B. R., Beck, P. B., Hyde, J. R., Bisagno, V., et al. (2014). Pedunculopontine nucleus gamma band activity-preconscious awareness, waking and REM sleep. Front. Neurol. 5:210. doi: 10.3389/fneur.2014.00210
56. Valencia, M., Chavez, M., Artieda, J., Bolam, J. P., and Mena-Segovia, J. (2014). Abnormal functional connectivity between motor cortex and pedunculopontine nucleus following chronic dopamine depletion. J. Neurophysiol. 111, 434-440. doi: 10.1152/jn.00555.2013
57. Wang, H. L., and Morales, M. (2009). Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur. J. Neurosci. 29, 340-358. doi: 10.1111/j.1460-9568.2008.06576.x
58. Williams, J. A., Comisarow, J., Day, J., Fibiger, H. C., and Reiner, P. B. (1994). State-dependent release of acetylcholine in rat thalamus measured by in vivo microdyalisis.J. Neurosci. 14, 5236-5242.
59. Winn, P. (2006). How best to consider the structure and function of the pedunculopontine tegmental nucleus: evidence from animal studies. J. Neurol. Sci.248, 234-250. doi: 10.1016/j.jns.2006.05.036
60. Ye, M., Hayar, A., and Garcia-Rill, E. (2009). Cholinergic responses and intrinsic membrane properties of developing thalamic parafascicular neurons. J. Neurophysiol.102, 774-785. doi: 10.1152/jn.91132.2008