Deep brain stimulation of different pedunculopontine targets in a novel rodent model of parkinsonism

Journal of Neuroscience

Volumn 35, Issue 12, 2015, Pages 4792-4803

  Gut, Nadine K ^a,b   Winn, Philip ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Basal ganglia; Cognition; Deep brain stimulation; Dopamine; Freezing of gait; Posture

Indexed keywords

DOPAMINE; LEVODOPA; IBOTENIC ACID; OXIDOPAMINE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BODY POSTURE; BRAIN DEPTH STIMULATION; CELL COUNT; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; GAIT; IMMUNOHISTOCHEMISTRY; MALE; MOTOR CONTROL; NONHUMAN; PARKINSONISM; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PRIORITY JOURNAL; RAT; TRAINING; ANIMAL; BODY EQUILIBRIUM; CHOLINERGIC NERVE CELL; DISEASE MODEL; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; PARKINSONIAN DISORDERS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CELL SURVIVAL; CHOLINERGIC NEURONS; DEEP BRAIN STIMULATION; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; GAIT; IBOTENIC ACID; LEVODOPA; MALE; OXIDOPAMINE; PARKINSONIAN DISORDERS; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; POSTURAL BALANCE; RATS;

EID: 84925847796     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3646-14.2015     Document Type: Article

References (82)

1. Alam M, Schwabe K, Krauss JK (2011) The pedunculopontine nucleus area: critical evaluation of interspecies differences relevant for its use as a target for deep brain stimulation. Brain 134:11–23. CrossRef Medline
2. Alderson HL, Faulconbridge LF, Gregory LP, Latimer MP, Winn P (2003) Behavioural sensitisation to repeated d-amphetamine: effects of excitotoxic lesions of the pedunculopontine tegmental nucleus. Neuroscience 118:311–315. CrossRef Medline
3. Alderson HL, Latimer MP, Blaha CD, Phillips AG, Winn P (2004) An examination of d-amphetamine self-administration in pedunculopontine tegmental nucleus-lesioned rats. Neuroscience 125:349–358. CrossRef Medline
4. Alderson HL, Latimer MP, Winn P (2006) Intravenous self-administration of nicotine is altered by lesions of the posterior, but not anterior, pedunculopontine tegmental nucleus. Eur J Neurosci 23:2169–2175. CrossRef Medline
5. Alderson HL, Latimer MP, Winn P (2008) A functional dissociation of the anterior and posterior pedunculopontine tegmental nucleus: excitotoxic lesions have differential effects on locomotion and the response to nicotine. Brain Struct Funct 213:247–253. CrossRef Medline
6. Alessandro S, Ceravolo R, Brusa L, Pierantozzi M, Costa A, Galati S, Placidi F, Romigi A, Iani C, Marzetti F, Peppe A (2010) Non-motor functions in parkinsonian patients implanted in the pedunculopontine nucleus: focus on sleep and cognitive domains. J Neurol Sci 289:44–48. CrossRef Medline
7. Aravamuthan BR, Bergstrom DA, French RA, Taylor JJ, Parr-Brownlie LC, Walters JR (2008) Altered neuronal activity relationships between the pedunculopontine nucleus and motor cortex in a rodent model of Parkinson’s disease. Exp Neurol 213:268 –280. CrossRef Medline
8. Aziz TZ, Davies L, Stein J, France S (1998) The role of descending basal ganglia connections to the brain stem in parkinsonian akinesia. Br J Neurosurg 12:245–249. CrossRef Medline
9. Ballanger B, Lozano AM, Moro E, van Eimeren T, Hamani C, Chen R, Cilia R, Houle S, Poon YY, Lang AE, Strafella AP (2009) Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson’s disease: a [(15)O] H2O PET study. Hum Brain Mapp 30:3901–3909. CrossRef Medline
10. Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson’s disease. Brain 124:2131–2146. CrossRef Medline
11. Brantley RK, Bass AH (1988) Cholinergic neurons in the brain of a teleost fish (Porichthys notatus) located with a monoclonal antibody to choline acetyltransferase. J Comp Neurol 275:87–105. CrossRef Medline
12. Breit S, Bouali-Benazzouz R, Benabid AL, Benazzouz A (2001) Unilateral lesion of the nigrostriatal pathway induces an increase of neuronal activity of the pedunculopontine nucleus, which is reversed by the lesion of the subthalamic nucleus in the rat. Eur J Neurosci 14:1833–1842. CrossRef Medline
13. Brooks DJ, Samuel M (2000) The effects of surgical treatment of Parkinson’s disease on brain function: PET findings. Neurology 55 [12 Suppl 6]:S52–S59. CrossRef Medline
14. Ceravolo R, Brusa L, Galati S, Volterrani D, Peppe A, Siciliano G, Pierantozzi M, Moschella V, Bonuccelli U, Stanzione P, Stefani A (2011) Low frequency stimulation of the nucleus tegmenti pedunculopontini increases cortical metabolism in parkinsonian patients. Eur J Neurol 18:842– 849. CrossRef Medline
15. Corrigall WA, Coen KM, Zhang J, Adamson KL (2001) GABA mechanisms in the pedunculopontine tegmental nucleus influence particular aspects of nicotine self-administration selectively in the rat. Psychopharmacology 158:190 –197. CrossRef Medline
16. Creese I, Iversen SD (1973) Blockage of amphetamine induced motor stimulation and stereotypy in the adult rat following neonatal treatment with 6-hydroxydopamine. Brain Res 55:369 –382. CrossRef Medline
17. Dellu F, Mayo W, Cherkaoui J, Le Moal M, Simon H (1991) Learning disturbances following excitotoxic lesion of cholinergic pedunculo-pontine nucleus in the rat. Brain Res 544:126 –132. CrossRef Medline
18. Diederich K, Koch M (2005) Role of the pedunculopontine tegmental nu cleus in sensorimotor gating and reward-related behavior in rats. Psychopharmacology 179:402– 408. CrossRef Medline
19. Fahn S (1995) The freezing phenomenon in Parkinsonism, negative motor phenomena. In: Advances in neurology, Vol. 67 (Fahn S, Hallett M, Luders HO, Marsden CD, eds), pp 53– 63. Philadelphia: Lippincott-Raven. CrossRef Medline
20. Ferraye MU, Debû B, Fraix V, Goetz L, Ardouin C, Yelnik J, Henry-Lagrange C, Seigneuret E, Piallat B, Krack P, Le Bas JF, Benabid AL, Chabardès S, Pollak P (2010) Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson’s disease. Brain 133:205–214. CrossRef Medline
21. Garcia-Rill E, Houser CR, Skinner RD, Smith W, Woodward DJ (1987) Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus. Brain Res Bull 18:731–738. CrossRef Medline
22. Garcia-Rill E, Simon C, Smith K, Kezunovic N, Hyde J (2011) The pedunculopontine tegmental nucleus: from basic neuroscience to neurosurgical applications: arousal from slices to humans: implications for DBS. J Neural Transm 118:1397–1407. CrossRef Medline
23. Hamers FP, Koopmans GC, Joosten EA (2006) CatWalk-assisted gait analysis in the assessment of spinal cord injury. J Neurotrauma 23:537–548. CrossRef Medline
24. Hirsch EC, Graybiel AM, Duyckaerts C, Javoy-Agid F (1987) Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc Natl Acad Sci U S A 84:5976 –5980. CrossRef Medline
25. Homs-Ormo S, Coll-Andreu M, Satorra-Marín N, Arévalo-García R, Morgado-Bernal I (2003) Effects of pedunculopontine tegmental nucleus lesions on emotional reactivity and locomotion in rats. Brain Res Bull 59:495–503. CrossRef Medline
26. Inglis WL, Dunbar JS, Winn P (1994a) Outflow from the nucleus accumbens to the pedunculopontine tegmental nucleus: a dissociation between locomotor activity and the acquisition of responding for conditioned reinforcement stimulated by d-amphetamine. Neuroscience 62:51–64. CrossRef Medline
27. Inglis WL, Allen LF, Whitelaw RB, Latimer MP, Brace HM, Winn P (1994b) 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 58:817–833. CrossRef Medline
28. Keating GL, Winn P (2002) Examination of the role of the pedunculopontine tegmental nucleus in radial maze tasks with or without a delay. Neuroscience 112:687– 696. CrossRef Medline
29. Kobayashi K, Hoshino K, Homma S, Takagi S, Norita M (2007) A possible monosynaptic pathway links the pedunculopontine tegmental nucleus to thalamostriatal neurons in the hooded rat. Arch Histol Cytol 70:207–214. CrossRef Medline
30. Kobayashi Y, Okada K (2007) Reward prediction error computation in the pedunculopontine tegmental nucleus neurons. Ann N Y Acad Sci 1104: 310 –323. CrossRef Medline
31. Kojima J, Yamaji Y, Matsumura M, Nambu A, Inase M, Tokuno H, Takada M, Imai H (1997) Excitotoxic lesions of the pedunculopontine tegmental nucleus produce contralateral hemiparkinsonism in the monkey. Neurosci Lett 226:111–114. CrossRef Medline
32. Lim AS, Moro E, Lozano AM, Hamani C, Dostrovsky JO, Hutchison WD, Lang AE, Wennberg RA, Murray BJ (2009) Selective enhancement of rapid eye movement sleep by deep brain stimulation of the human pons. Ann Neurol 66:110 –114. CrossRef Medline
33. MacLaren DA, Santini JA, Russell AL, Markovic T, Clark SD (2014) Deficits in motor performance after pedunculopontine lesions in rats - impairment depends on demands of task. Eur J Neurosci 40:3224–3236. CrossRef Medline
34. Marín O, Smeets WJ, González A (1997) Distribution of choline acetyltransferase immunoreactivity in the brain of anuran (Rana perezi, Xenopus laevis) and urodele (Pleurodeles waltl) amphibians. J Comp Neurol 382:499 –534. CrossRef Medline
35. Martinez-Gonzalez C, Bolam JP, Mena-Segovia J (2011) Topographical organization of the pedunculopontine nucleus. Front Neuroanat 5:22. CrossRef Medline
36. Martinez-Gonzalez C, Wang HL, Micklem BR, Bolam JP, 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. CrossRef Medline
37. Maskos U (2008) The cholinergic mesopontine tegmentum is a relatively neglected nicotinic master modulator of the dopaminergic system: relevance to drugs of abuse and pathology. Br J Pharmacol 153 [Suppl 1]: S438 –S445. CrossRef
38. Mazzone P, Lozano A, Stanzione P, Galati S, Scarnati E, Peppe A, Stefani A (2005) Implantation of human pedunculopontine nucleus: a safe and clinically relevant target in Parkinson’s disease. Neuroreport 16:1877– 1881. CrossRef Medline
39. Medina L, Reiner A (1994) Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342:497–537. CrossRef Medline
40. Mena-Segovia J, Micklem BR, Nair-Roberts RG, Ungless MA, Bolam JP (2009) GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J Comp Neurol 515:397–408. CrossRef Medline
41. Mena-Segovia J, Bolam JP (2011) Phasic modulation of cortical highfrequency oscillations by pedunculopontine neurons. Prog Brain Res 193: 85–92. CrossRef Medline
42. Mena-Segovia J, Winn P, Bolam JP (2008a) Cholinergic modulation of midbrain dopaminergic systems. Brain Res Rev 58:265–271. CrossRef Medline
43. Mena-Segovia J, Sims HM, Magill PJ, Bolam JP (2008b) Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J Physiol 586:2947–2960. CrossRef Medline
44. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185–1201. CrossRef Medline
45. Mesulam MM, Geula C, Bothwell MA, Hersh LB (1989) Human reticular formation: cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J Comp Neurol 283:611– 633. CrossRef Medline
46. Mitchell IJ, Clarke CE, Boyce S, Robertson RG, Peggs D, Sambrook MA, Crossman AR (1989) Neural mechanisms underlying parkinsonian symptoms based upon regional uptake of 2-deoxyglucose in monkeys exposed to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neuroscience 32:213–226. CrossRef Medline
47. Munro-Davies LE, Winter J, Aziz TZ, Stein JF (1999) The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia. Exp Brain Res 129:511–517. CrossRef Medline
48. Nandi D, Aziz TZ, Giladi N, Winter J, Stein JF (2002) Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain 125:2418 –2430. CrossRef Medline
49. Okada K, Kobayashi Y (2013) Reward prediction-related increases and decreases in tonic neuronal activity of the pedunculopontine tegmental nucleus. Front Integr Neurosci 7:36. CrossRef Medline
50. Okada K, Toyama K, Inoue Y, Isa T, Kobayashi Y (2009) Different pedunculopontine tegmental neurons signal predicted and actual task rewards. J Neurosci 29:4858 – 4870. CrossRef Medline
51. Olmstead MC, Franklin KB (1994) Lesions of the pedunculopontine tegmental nucleus block drug-induced reinforcement but not amphetamine-induced locomotion. Brain Res 638:29–35. CrossRef Medline
52. Olmstead MC, Munn EM, Franklin KB, Wise RA (1998) Effects of pedunculopontine tegmental nucleus lesions on responding for intravenous heroin under different schedules of reinforcement. J Neurosci 18:5035–5044. Medline
53. Orieux G, Francois C, Féger J, Yelnik J, Vila M, Ruberg M, Agid Y, Hirsch EC (2000) Metabolic activity of excitatory parafascicular and pedunculopontine inputs to the subthalamic nucleus in a rat model of Parkinson’s disease. Neuroscience 97:79 – 88. CrossRef Medline
54. Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson’s disease. Brain 123:1767–1783. CrossRef Medline
55. Pan WX, Hyland BI (2005) Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J Neurosci 25:4725– 4732. CrossRef Medline
56. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. San Diego: Elsevier Academic. CrossRef Medline
57. PetrovicJ, CiricJ, LazicK, Kalauzi A, SaponjicJ (2013) Lesionofthepedunculopontinetegmental nucleusinrataugmentscortical activationanddisturbssleep/wake state transitions structure. Exp Neurol 247:562–571. CrossRef Medline
58. Pienaar IS, Elson JL, Racca C, Nelson G, Turnbull DM, Morris CM (2013) Mitochondrial abnormality associates with type-specific neuronal loss and cell morphology changes in the pedunculopontine nucleus in Parkinson disease. Am J Pathol 183:1826 –1840. CrossRef Medline
59. Plaha P, Gill SS (2005) Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson’s disease. Neuroreport 16:1883–1887. CrossRef Medline
60. Pötter-Nerger M, Volkmann J (2013) Deep brain stimulation for gait and postural symptoms in Parkinson’s disease. Mov Disord 28:1609 –1615. CrossRef Medline
61. Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Berg man H, Agid Y, DeLong MR, Obeso JA (2010) Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nat Rev Neurosci 11:760 –772. CrossRef Medline
62. Rinne JO, Ma SY, Lee MS, Collan Y, Röyttä M (2008) Loss of cholinergic neurons in the pedunculopontine nucleus in Parkinson’s disease is related to disability of the patients. Parkinsonism Relat Disord 14:553–557. CrossRef Medline
63. Ros H, Magill PJ, Moss J, Bolam JP, Mena-Segovia J (2010) Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states. Neuroscience 170:78 –91. CrossRef Medline
64. Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259: 483–528. CrossRef Medline
65. Samson HH, Chappell A (2001) Injected muscimol in pedunculopontine tegmental nucleus alters ethanol self-administration. Alcohol 23:41– 48. CrossRef Medline
66. Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE (2010) Sleep state switching. Neuron 68:1023–1042. CrossRef Medline
67. Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N (2003) Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol 10:391–398. CrossRef Medline
68. Skinner RD, Kinjo N, Henderson V, Garcia-Rill E (1990) Locomotor projections from the pedunculopontine nucleus to the spinal cord. Neuroreport 1:183–186. CrossRef Medline
69. Stefani A, Lozano AM, Peppe A, Stanzione P, Galati S, Tropepi D, Pierantozzi M, Brusa L, Scarnati E, Mazzone P (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease. Brain 130:1596 –1607. CrossRef Medline
70. Stefani A, Peppe A, Galati S, Bassi MS, D’Angelo V, Pierantozzi M (2013) The serendipity case of the pedunculopontine nucleus low-frequency brain stimulation: chasing a gait response, finding sleep, and cognition improvement. Front Neurol 4:68. CrossRef Medline
71. Steiniger B, Kretschmer BD (2004) Effects of ibotenate pedunculopontine tegmental nucleus lesions on exploratory behaviour in the open field. Behav Brain Res 151:17–23. CrossRef Medline
72. Stephenson-Jones M, Samuelsson E, Ericsson J, Robertson B, Grillner S (2011) Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr Biol 21:1081–1091. CrossRef Medline
73. Swerdlow NR, Koob GF (1987) Lesions of the dorsomedial nucleus of the thalamus, medial prefrontal cortex and pedunculopontine nucleus: effects on locomotor activity mediated by nucleus accumbens-ventral pallidal circuitry. Brain Res 412:233–243. CrossRef Medline
74. Taylor CL, Kozak R, Latimer MP, Winn P (2004) Effects of changing reward on performance of the delayed spatial win-shift radial maze task in pedunculopontine tegmental nucleus lesioned rats. Behav Brain Res 153: 431– 438. CrossRef Medline
75. Thevathasan W, Silburn PA, Brooker H, Coyne TJ, Khan S, Gill SS, Aziz TZ, Brown P (2010) The impact of low-frequency stimulation of the pedunculopontine nucleus region on reaction time in parkinsonism. J Neurol Neurosurg Psychiatry 81:1099 –1104. CrossRef Medline
76. Thompson JA, Felsen G (2013) Activity in mouse pedunculopontine tegmental nucleus reflects action and outcome in a decision-making task. J Neurophysiol 110:2817–2829. CrossRef Medline
77. Wang HL, 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. CrossRef Medline
78. Whishaw IQ, Cioe JD, Previsich N, Kolb B (1977) The variability of the interaural line vs the stability of bregma in rat stereotaxic surgery. Physiol Behav 19:719 –722. CrossRef Medline
79. Wilson DI, MacLaren DA, Winn P (2009) Bar pressing for food: differential consequences of lesions to the anterior versus posterior pedunculopontine. Eur J Neurosci 30:504 –513. CrossRef Medline
80. 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. CrossRef Medline
81. Winn P (2008) Experimental studies of pedunculopontine functions: are they motor, sensory or integrative? Parkinsonism Relat Disord 14 [Suppl 2]:S194–S198. CrossRef Medline
82. Zrinzo L, Zrinzo LV, Hariz M (2007) The pedunculopontine and peripeduncular nuclei: a tale of two structures. Brain 130:e73; author reply e74. CrossRef Medline