Brainstem control of locomotion and muscle tone with special reference to the role of the mesopontine tegmentum and medullary reticulospinal systems

Abstract

The lateral part of the mesopontine tegmentum contains functionally important structures involved in the control of posture and gait. Specifically, the mesencephalic locomotor region, which may consist of the cuneiform nucleus and pedunculopontine tegmental nucleus (PPN), occupies the interest with respect to the pathophysiology of posture-gait disorders. The purpose of this article is to review the mechanisms involved in the control of postural muscle tone and locomotion by the mesopontine tegmentum and the pontomedullary reticulospinal system. To make interpretation and discussion more robust, the above issue is considered largely based on our findings in the experiments using decerebrate cat preparations in addition to the results in animal experimentations and clinical investigations in other laboratories. Our investigations revealed the presence of functional topographical organizations with respect to the regulation of postural muscle tone and locomotion in both the mesopontine tegmentum and the pontomedullary reticulospinal system. These organizations were modified by neurotransmitter systems, particularly the cholinergic PPN projection to the pontine reticular formation. Because efferents from the forebrain structures as well as the cerebellum converge to the mesencephalic and pontomedullary reticular formation, changes in these organizations may be involved in the appropriate regulation of posture-gait synergy depending on the behavioral context. On the other hand, abnormal signals from the higher motor centers may produce dysfunction of the mesencephalic-reticulospinal system. Here we highlight the significance of elucidating the mechanisms of the mesencephalic-reticulospinal control of posture and locomotion so that thorough understanding of the pathophysiological mechanisms of posture-gait disorders can be made.

References 263

1. 1.

   Adkins R, Cegner MR, Rafuse DD. Differential effects of lesions of the anterior posterior sigmoid gyri in cats. Brain Res. 1971;30:411-414.

   Not in our library10.1016/0006-8993(71)90092-8 (opens in a new tab)

2. 2.

   Alam M, Schwabe K, Krauss JK. The pedunculopontine nucleus area: critical evaluation of interspecies differences relevant for its use as a target for deep brain stimulation. Brain. 2011;134(Pt 1):11-23.

   Not in our library10.1093/brain/awq322 (opens in a new tab)

3. 3.

   Allcock LM, Rowan EN, Steen IN, Wesnes K, Kenny RA, Burn DJ. Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat Disord. 2009;15(2):110-115.

   Not in our library10.1016/j.parkreldis.2008.03.010 (opens in a new tab)

4. 4.

   Amemiya M, Yamaguchi T. Fictive locomotion of the forelimb evoked by stimulation of the mesencephalic locomotor region in the decerebrate cat. Neurosci Lett. 1984;50:91-96.

   Not in our library10.1016/0304-3940(84)90468-3 (opens in a new tab)

5. 5.

   Antonino-Green DM, Cheng J, Magnuson DS. Neurons labeled from locomotor-related ventrolateral funiculus stimulus sites in the neonatal rat spinal cord. J Comp Neurol. 2002;442:226-238.

   Not in our library10.1002/cne.10081 (opens in a new tab)

6. 6.

   Aravamuthan BR, McNab JA, Miller KL, Rushworth M, Jenkinson N, Stein JF, Aziz TZ. Cortical and subcortical connections within the pedunculopontine nucleus of the primate Macaca mulatta determined using probabilistic diffusion tractography. J Clin Neurosci. 2009;16:413-420.

   Not in our library10.1016/j.jocn.2008.03.018 (opens in a new tab)

7. 7.

   Armstrong DM. Supraspinal contributions to the initiation and control of locomotion in the cat. Prog Neurobiol. 1986;26:273-361.

   Not in our library10.1016/0301-0082(86)90021-3 (opens in a new tab)

8. 8.

   Arnulf I, Ferraye M, Fraix V, Benabid AL, Chabardès S, Goetz L, Pollak P, Debû B. Sleep induced by stimulation in the human pedunculopontine nucleus area. Ann Neurol. 2010;67:546-549.

   Not in our library10.1002/ana.21912 (opens in a new tab)

9. 9.

   Asanome M, Matsuyama K, Mori S. Augmentation of postural muscle tone induced by the stimulation of the descending fibers in the midline area of the cerebellar white matter in the acute decerebrate cat. Neurosci Res. 1998;30:257-269.

   Not in our library10.1016/s0168-0102(98)00006-6 (opens in a new tab)

10. 10.

    Baghdoyan HA, Rodrigo-Angulo ML, McCarley RW, Hobson JA. A neuroanatomical gradient in the pontine tegmentum for the cholinoceptive induction of desynchronized sleep signs. Brain Res. 1987;414:245-261.

    Not in our library10.1016/0006-8993(87)90005-9 (opens in a new tab)

11. 11.

    Beckstead RM, Domesick VB, Nauta WJ. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 1979;175:191-217.

    Not in our library10.1016/0006-8993(79)91001-1 (opens in a new tab)

12. 12.

    Benarroch EE. Pedunculopontine nucleus: functional organization and clinical implications. Neurology. 2013;80:1148-1155.

    Not in our library10.1212/wnl.0b013e3182886a76 (opens in a new tab)

13. 13.

    Bianchi A, Gestreau C. The brainstem respiratory network: an overview of a half century of research. Respir Physiol Neurobiol. 2009;168:4-12.

    Not in our library10.1016/j.resp.2009.04.019 (opens in a new tab)

14. 14.

    Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH. Prospective assessment of falls in Parkinson’s disease. J Neurol. 2001;248:950-958.

    Not in our library10.1007/s004150170047 (opens in a new tab)

15. 15.

    Bohnen NI, Albin RL. The cholinergic system and Parkinson disease. Behav Brain Res. 2011;221:564-573.

    Not in our library10.1016/j.bbr.2009.12.048 (opens in a new tab)

16. 16.

    Bohnen NI, Frey KA, Studenski S, Kotagal V, Koeppe RA, Scott PJ, Albin RL, Müller ML. Gait speed in Parkinson disease correlates with cholinergic degeneration. Neurol. 2013;81(18):1611-1616.

    Not in our library10.1212/wnl.0b013e3182a9f558 (opens in a new tab)

17. 17.

    Bohnen NI, Kaufer DI, Ivanco LS, Lopresti B, Koeppe RA, Davis JG, Mathis CA, Moore RY, DeKosky ST. Cortical cholinergic function is more severely affected in parkinsonian dementia than in Alzheimer disease: an in vivo positron emission tomographic study. Arch Neurol. 2003;60(12):1745-1748.

    Not in our library10.1001/archneur.60.12.1745 (opens in a new tab)

18. 18.

    Bohnen NI, Müller ML, Koeppe RA, Studenski SA, Kilbourn MA, Frey KA, Albin RL. History of falls in Parkinson disease is associated with reduced cholinergic activity. Neurology. 2009;73:1670-1676.

    Not in our library10.1212/wnl.0b013e3181c1ded6 (opens in a new tab)

19. 19.

    Bohnen NI, Müller ML, Kotagal V, Koeppe RA, Kilbourn MR, Gilman S, Albin RL, Frey KA. Heterogeneity of cholinergic denervation in Parkinson’s disease without dementia. J Cereb Blood Flow Metab. 2012;32(8):1609-1617.

    Not in our library10.1038/jcbfm.2012.60 (opens in a new tab)

20. 20.

    Brodal A. Neurological anatomy in relation to Clinical Medicine. 1981;394-447.

    Not in our library

21. 21.

    Brooks VB, Storney SDJr. Motor mechanisms; the role of the pyramidal system in motor control. Annu Rev Physiol. 1971;33:337-392.

    Not in our library10.1146/annurev.ph.33.030171.002005 (opens in a new tab)

22. 22.

    Brudzyński SM, Mogenson GJ. Association of the mesencephalic locomotor region with locomotor activity induced by injections of amphetamine into the nucleus accumbens. Brain Res. 1985;334:77-84.

    Not in our library10.1016/0006-8993(85)90569-4 (opens in a new tab)

23. 23.

    Brudzynski SM, Houghton PE, Brownlee RD, Mogenson GJ. Involvement of neuronal cell bodies of the mesencephalic locomotor region in the initiation of locomotor activity of freely behaving rats. Brain Res Bull. 1986;16:377-381.

    Not in our library10.1016/0361-9230(86)90059-6 (opens in a new tab)

24. 24.

    Brudzynski SM, Wu M, Mogenson GJ. Decreases in rat locomotor activity as a result of changes in synaptic transmission to neurons within the mesencephalic locomotor region. Can J Physiol Pharmacol. 1993;71:394-406.

    Not in our library10.1139/y93-060 (opens in a new tab)

25. 25.

    Büttner U, Glasauer S, Glonti L, Guan Y, Kipiani E, Kleine J, Siebold C, Tchelidze T, Wilden A. Multimodal signal integration in vestibular neurons of the primate fastigial nucleus. Ann N Y Acad Sci. 2003;1004:241-251.

    Not in our library10.1196/annals.1303.021 (opens in a new tab)

26. 26.

    Cavdar S, Onat FY, Yananli HR, Sehirli US, Tulay C, Saka E, Gürdal E. Cerebellar connections to the rostral reticular nucleus of the thalamus in the rat. J Anat. 2002;201(6):485-491.

    Not in our library10.1046/j.1469-7580.2002.00119.x (opens in a new tab)

27. 27.

    Chan SH, Barnes CD. Postsynaptic effects evoked from brain stem reticular formation in lumbar cord and their temporal correlations with a presynaptic mechanism. Arch Ital Biol. 1974;112:81-97.

    Not in our library

28. 28.

    Chase MH, Hobson JA, Brazier MAB. The motor functions of the reticular formation are multifaceted and state-determined. The reticular formation revisited. 1980;449-472.

    Not in our library

29. 29.

    Chase MH, Morales FR. The atonia and myoclonia of active (REM) sleep. Annu Rev Psychol. 1990;41:557-584.

    Not in our library10.1146/annurev.ps.41.020190.003013 (opens in a new tab)

30. 30.

    Chase MH, Wills N. Brain stem control of masseteric reflex activity during sleep and wakefulness: medulla. Exp Neurol. 1979;64:118-131.

    Not in our library10.1016/0014-4886(79)90009-8 (opens in a new tab)

31. 31.

    Chase MH, Morales FR, Boxer P, Fung SJ, Soja PJ. Effect of stimulation of the nucleus reticularis gigantocellularis on the membrane potential of cat lumbar motoneurons during sleep and wakefulness. Brain Res. 1986;386:237-244.

    Not in our library10.1016/0006-8993(86)90160-5 (opens in a new tab)

32. 32.

    Chastan N, Westby GW, Yelnik J, Bardinet E, Do MC, Agid Y, Welter ML. Effects of nigral stimulation on locomotion and postural stability in patients with Parkinson’s disease. Brain. 2009;132:172-184.

    Not in our library10.1093/brain/awn294 (opens in a new tab)

33. 33.

    Clements JR, Grant S. Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci Lett. 1990;120:70-73.

    Not in our library10.1016/0304-3940(90)90170-e (opens in a new tab)

34. 34.

    Coffman KA, Dum RP, Strick PL. Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex. Proc Natl Acad Sci USA. 2011;108(38):16068-16073.

    Not in our library10.1073/pnas.1107904108 (opens in a new tab)

35. 35.

    Coles SK, Iles JF, Nicolopoulos-Stournaras S. The mesencephalic centre controlling locomotion in the rat. Neuroscience. 1989;28:149-157.

    Not in our library10.1016/0306-4522(89)90239-x (opens in a new tab)

36. 36.

    Datta S. Evidence that REM sleep is controlled by the activation of brain stem pedunculopontine tegmental kainate receptor. J Neurophysiol. 2002;87:1790-1978.

    Not in our library10.1152/jn.00763.2001 (opens in a new tab)

37. 37.

    Dautan D, Huerta-Ocampo I, Witten IB, Deisseroth K, Bolam JP, Gerdjikov T, Mena-Segovia J. A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J Neurosci. 2014;34(13):4509-4518.

    Not in our library10.1523/jneurosci.5071-13.2014 (opens in a new tab)

38. 38.

    DeLong MR, Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch Neurol. 2007;64:20-24.

    Not in our library10.1001/archneur.64.1.20 (opens in a new tab)

39. 39.

    Depoortere R, Di Scala G, Sandner G. Treadmill locomotion and aversive effects induced by electrical stimulation of the mesencephalic locomotor region in the rat. Brain Res Bull. 1990;25:723-727.

    Not in our library10.1016/0361-9230(90)90049-6 (opens in a new tab)

40. 40.

    Douglas JR, Noga BR, Dai X, Jordan LM. The effects of intrathecal administration of excitatory amino acid agonists and antagonists on the initiation of locomotion in the adult cat. J Neurosci. 1993;13:990-1000.

    Not in our library10.1523/jneurosci.13-03-00990.1993 (opens in a new tab)

Cited by papers we hold 3

• Motoric Cognitive Risk Syndrome: Symptoms, Pathology, Diagnosis, and Recovery · 2022
  Not checked
• MR Tractography-Based Targeting and Physiological Identification of the Cuneiform Nucleus for Directional DBS in a Parkinson’s Disease Patient With Levodopa-Resistant Freezing of Gait · 2021
  Not checked
• Reticulospinal Systems for Tuning Motor Commands · 2018
  No notice

Questions about this paper

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.