Lesion of the pedunculopontine tegmental nucleus in rat augments cortical activation and disturbs sleep/wake state transitions structure

Experimental Neurology

Volumn 247, Issue , 2013, Pages 562-571

  Petrovic, Jelena ^a   Ciric, Jelena ^a   Lazic, Katarina ^a   Kalauzi, Aleksandar ^b   Saponjic, Jasna ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Cholinergic neurons; Electroencephalography; Ibotenic acid; Lesion; Pedunculopontine tegmental nucleus; Rat; Sleep wake states; Sleep wake states transitions

Indexed keywords

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; BETA RHYTHM; BRAIN STEM INJURY; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DELTA RHYTHM; ELECTROENCEPHALOGRAM; ELECTROMYOGRAM; FREQUENCY MODULATION; GAMMA RHYTHM; MALE; NERVE CELL DEGENERATION; NONHUMAN; NONREM SLEEP; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PRIORITY JOURNAL; RAT; REM SLEEP; SIGNAL PROCESSING; SLEEP WAKING CYCLE; THETA RHYTHM;

CHOLINERGIC NEURONS; ELECTROENCEPHALOGRAPHY; IBOTENIC ACID; LESION; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; RAT; SLEEP-WAKE STATES; SLEEP-WAKE STATES TRANSITIONS;

ANIMALS; CEREBRAL CORTEX; DELTA RHYTHM; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; EXCITATORY AMINO ACID AGONISTS; IBOTENIC ACID; MALE; NADPH DEHYDROGENASE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; RATS; RATS, WISTAR; SLEEP; SLEEP DISORDERS; WAKEFULNESS;

EID: 84881370170     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.02.007     Document Type: Article

References (58)

1. Boeve B.F., Silber M.H., Saper C.B., Ferman T.J., Dickson D.W., Parisi J.E., Benarroch E.E., Ahlskog J.E., Smith G.E., Caselli R.C., Tippman-Peikert M., Olson E.J., Lin S.C., Young T., Wszolek Z., Schenck C.H., Mahowald M.W., Castillo P.R., Del Tredici K., Braak H. Pathophysiology of REM sleep behaviour disorder and relevance to neurodegenerative disease. Brain Rev. 2007, 130:2770-2788.
2. Bohnen N.I., Müller M.I., Koeppe R.A., Studenski S.A., Kilbourn M.A., Fey K.A., Albin R.L. History of falls in Parkinson disease is associated with reduced cholinergic activity. Neurology 2009, 73:1670-1676.
3. Bohnnen N.I., Albin R.L. The cholinergic system and Parkinson disease. Behav. Brain Res. 2011, 221:564-573.
4. Boucetta S., Jones B. Activity profiles of cholinergic and intermingled GABAergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-anesthetized rats. J. Neurosci. 2009, 29:4664-4674.
5. Bringmann A. Different functions of rat's pedunculopontine tegmental nucleus are reflected in cortical EEG. Neuroreport 1995, 15:2065-2068.
6. Bringmann A. Nicotine affects the occipital theta rhythm after lesion of the pedunculopontine tegmental nucleus in rats. Neuropsychobiology 1997, 35:102-107.
7. Buzsaki G., Bickford R.G., Ponomareff G., Thai L.J., Mandel R., Gage F.H. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 1988, 8:4007-4026.
8. Carley W.D., Radulovacki M. Pathophysiology of sleep-related breathing disorders: unanswered questions. Sleep-related Breathing Disorders: Experimental Models and Therapeutic Potential 2003, 3-16. Marcel Dekker Inc., New York-Basel. D.W. Carley, M. Radulovacki (Eds.).
9. Chung K.A., Lobb B.M., Nutt J.G., Horak F. Cholinergic augmentation in frequently fallings subjects with Parkinson's disease. Mov. Disord. 2009, 24(Suppl. 1):S259.
10. Datta S. Neuronal activity in the peribrachial area: relationship to behavioral state control. Neurosci. Biobehav. Rev. 1995, 19:67-84.
11. Datta S. Cellular basis of pontine ponto-geniculo-occipital wave generation and modulation. Cell. Mol. Neurobiol. 1997, 17:341-365.
12. Datta S. Evidence that REM sleep is controlled by activation of brain stem pedunculopontine tegmental kainate receptor. J. Neurophysiol. 2002, 87:1790-1798.
13. Datta S., MacLean R.R. Neurobiological mechanisms for the regulation of mammalian sleep-wake behavior: reinterpretation of historical evidence and inclusion of contemporary cellular and molecular evidence. Neurosci. Biobehav. Rev. 2007, 31:775-824.
14. Datta S., Siwek D.F. Excitation of the brain stem pedunculopontine tegmentum cholinergic cells induces wakefulness and REM sleep. J. Neurophysiol. 1997, 77:2975-2988.
15. Datta S., Spoley E.E., Patterson E.H. Microinjection of glutamate into pedunculopontine tegmentum induces REM sleep and wakefulness in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R752-R759.
16. Dringenberg H.C., Olmstead M.C. Integrated contributions of basal forebrain and thalamus to neocortical activation elicited by pedunculopontine tegmental stimulation in urethane-anesthetized rats. Neuroscience 2003, 119:839-853.
17. Garcia-Rill E. The pedunculopontine nucleus. Prog. Neurobiol. 1991, 36:363-389.
18. Hobson J.A., Pace-Schott E.F. The cognitive neuroscience of sleep: neuronal systems, consciousness and learning. Nat. Rev. 2002, 3:679-693.
19. Inglis W.L., Semba K. Discriminable excitotoxic effects of ibotenic acid, AMPA, NMDA and quinolonic acid in the rat laterodorsal tegmental nucleus. Brain Res. 1997, 755:17-27.
20. Inglis W.L., Allen L.F., Whitelaw R.B., Latimer M.P., Brace H.M., Winn P. An investigation into the role of the pedunculopontine tegmental nucleus in the mediation of locomotion and orofacial stereotypy induced by D-amphetamine and apomorphine in the rat. Neuroscience 1994, 58:817-833.
21. Jones B.E. Arousal systems. Front. Biosci. 2003, 8:s438-s451.
22. Kleiner S., Bringmann A. Nucleus basalis magnocellularis and pedunculopontine tegmental nucleus: control of slow EEG waves in rats. Arch. Ital. Biol. 1996, 134:153-167.
23. Kotagal V., Albin R.L., Müller M.L.T.M., Koeppe R.A., Chervin R.D., Frey K.A., Bohnen N.I. Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann. Neurol. 2012, 7:560-568.
24. Kotagal V., Müller M.L.T.M., Kaufer D.I., Koeppe R.A., Bohnen N.I. Thalamic cholinergic innervation is spared in Alzheimer disease compared to parkinsonian disorders. Neurosci. Lett. 2012, 514:169-172.
25. Loiser B.J., Semba K. Dual projections of single cholinergic and aminergic brainstem neurons to the thalamus and basal forebrain in the rat. Brain Res. 1993, 604:41-52.
26. Lu J., Sherman D., Devor M., Saper C.B. A putative flip-flop switch for control of REM sleep. Nature 2006, 441:589-594.
27. Lydic R., Baghdoyan H.A. Pedunculopontine stimulation alters respiration and increases Ach release in the pontine reticular formation. Am. J. Physiol. 1993, 264:R544-R554.
28. Maloney K.J., Cape E.G., Gotman J., Jones B.E. High frequency gamma electroencephalogram activity in association with sleep-wake states and spontaneous behaviors in the rat. Neuroscience 1997, 76:541-555.
29. McCarley R.W., Hobson J.A. Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 1975, 189:58-60.
30. Mena-Segovia J., Sims H.M., Magill P.J., Bolam J.P. Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J. Physiol. 2008, 586:2947-2960.
31. Pace-Schott E.F., Hobson J.A. Basic mechanisms of sleep: new evidence on the neuroanatomy and neuromodulation of the NREM-REM cycle. Neuropsychopharmacology: The Fifth Generation of Progress 2002, 1859-1877. Lippincott Williams and Wilkins, Philadelphia, USA. K.L. Davis, D. Charney, J.T. Coyle, C. Nemeroff (Eds.).
32. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Academic Press, San Diego, USA. 5th ed.
33. Paxinos G., Watson C., Carrive P., Kirkcaldie M., Ashwell K.W.S. Chemoarchitectonic Atlas of The Rat Brain 2009, Academic Press, London, UK. Second edition.
34. Radulovacki M., Pavlovic S., Saponjic J., Carley D.W. Modulation of reflex and sleep related apnea by pedunculopontine tegmental and intertrigeminal neurons. Respir. Physiol. Neurobiol. 2004, 143:293-306.
35. Raggi A., Ferri R. Sleep disorders in neurodegenerative diseases. Eur. J. Neurol. 2010, 17:1326-1338.
36. Rye D.B. Contributions of the pedunculopontine region to normal and altered REM sleep. Sleep 1997, 20:757-788.
37. Sabbatini M., Bronzetti E., Felici L., Fringuelli Ch., Sagratella S., Amenta F. NADPH-diaphorase histochemistry in the rat cerebral cortex and hippocampus: effect of electrolytic lesions of the nucleus basalis magnocellularis. Mech. Ageing Dev. 1999, 107:147-157.
38. Saper C.B., Loewy A.D. Projections of the pedunculopontine tegmental nucleus in the rat: evidence for additional extrapyramidal circuitry. Brain Res. 1982, 252:367-372.
39. Saponjic J., Radulovacki M., Carley D.W. Respiratory pattern modulation by the pedunculopontine tegmental nucleus. Respir. Physiol. Neurobiol. 2003, 138:223-237.
40. Saponjic J., Cvorovic J., Radulovacki M., Carley D.W. Serotonin and noradrenaline modulate respiratory pattern disturbance evoked by glutamate injection into pedunculopontine tegmentum of anesthetized rats. Sleep 2005, 28:560-570.
41. Saponjic J., Radulovacki M., Carley D.W. Injection of glutamate into the pedunculopontine tegmental nuclei of anesthetized rat causes respiratory dysrhythmia and alters EEG and EMG power. Sleep Breath. 2005, 9:82-91.
42. Saponjic J., Radulovacki M., Carley D.W. Modulation of respiratory pattern and upper airway muscle activity by the pedunculopontine tegmentum: role of NMDA receptors. Sleep Breath. 2006, 10:195-202.
43. Saponjic J., Radulovacki M., Carley D.W. Monoaminergic system lesions increase post-sigh respiratory pattern disturbance during sleep in rats. Physiol. Behav. 2007, 90:1-10.
44. Sarter M., Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 2000, 95:933-952.
45. Semba K. Aminergic and cholinergic afferents to REM sleep induction regions of the pontine reticular formation in the rat. J. Comp. Neurol. 1993, 330:543-556.
46. Simic G., Stanic G., Mladinov M., Jovanov-Milosevic N., Kostovic I., Hof P.R. Does Alzheimer's disease begin in the brainstem?. Neuropathol. Appl. Neurobiol. 2009, 35:532-554.
47. Steriade M. Corticothalamic resonance, states of vigilance and mentation. Neuroscience 2000, 101:243-276.
48. Steriade M. The corticothalamic system in sleep. Front. Biosci. 2003, 8:878-899.
49. Takakusaki K., Habaguchi T., Saitoh K., Kohyama J. Changes in the excitability of hindlimb motoneurons during muscular atonia induced by stimulating the pedunculopontine tegmental nucleus in cats. Neuroscience 2004, 124:467-480.
50. Timofeev I., Grenier F., Bazhenov M., Sjenowski T.J., Steriade M. Origin of slow oscillations in deafferented cortical slabs. Cereb. Cortex 2000, 10:1185-1199.
51. Vanderwolf C.H., Stewart D.J. Thalamic control and neocortical activation: a critical re-evaluation. Brain Res. Bull. 1993, 20:529-538.
52. Vertes R.P. Brainstem control of the events of REM sleep. Prog. Neurobiol. 1984, 22:241-288.
53. Vincent S.R. Histochemistry of endogenous enzymes. Experimental Neuroanatomy: A Practical Approach 1992, 153-171. Oxford University Press, Oxford-New York-Tokyo. J.P. Bloam (Ed.).
54. Vincent S.R., Satoh K., Armstrong D.M., Fibiger H.C. NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci. Lett. 1983, 143:31-36.
55. Whitwell J.L., Weigand S.D., Shiung M.M., Boeve B.F., Ferman T.J., Smith G.E., Knopman D.S., Petersen R.C., Benarroch E.E., Josephs K.A., Jack C.R. Focal atrophy in dementia with Lewy bodies on MRI: a distinct pattern from Alzheimer's disease. Brain 2007, 130:708-719.
56. Williams J.A., Comisarow J., Day J., Fibiger H.C., Reiner P.B. State-dependent release of acetylcholine in rat thalamus measured by in vivo microdialysis. J. Neurosci. 1994, 14:5236-5242.
57. Winn P. How best to consider the structure and function of the pedunculopontine tegmental nucleus: evidence from animal studies. J. Neurol. Sci. 2006, 248:234-250.
58. Yan M.M., Xu X.H., Huang Z.L., Yao M.H., Urade Y., Qu W.M. Selection of optimal epoch duration in assessment of rodent sleep-wake profiles. Sleep Biol. Rhythms 2011, 9:46-55.