Subthalamic nucleus activity in the awake hemiparkinsonian rat: Relationships with motor and cognitive networks

Journal of Neuroscience

Volumn 35, Issue 17, 2015, Pages 6918-6930

  Delaville, Claire ^a   McCoy, Alex J ^a   Gerber, Colin M ^a   Cruz, Ana V ^a   Walters, Judith R ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Beta oscillation; Dopamine; Gamma oscillations; Medial prefrontal cortex; Parkinson s disease; Subthalamic nucleus

Indexed keywords

APOMORPHINE; LEVODOPA; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ADRENERGIC RECEPTOR STIMULATING AGENT; ANTIPARKINSON AGENT; BENZAZEPINE DERIVATIVE; DOPAMINE RECEPTOR BLOCKING AGENT; OXIDOPAMINE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ARTICLE; COGNITION; HISTOLOGY; IMMUNOCHEMISTRY; MALE; MEDIAL PREFRONTAL CORTEX; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE CELL NETWORK; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; RAT; SCORING SYSTEM; SUBTHALAMIC NUCLEUS; TASK PERFORMANCE; TREADMILL TEST; ACTION POTENTIAL; ANIMAL; CHEMICALLY INDUCED; COGNITION DISORDERS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; EVOKED RESPONSE; HEMISPHERIC DOMINANCE; LONG EVANS RAT; METABOLISM; MOTOR ACTIVITY; PARKINSONIAN DISORDERS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TIME; WAKEFULNESS;

ACTION POTENTIALS; ADRENERGIC AGENTS; ANIMALS; ANTIPARKINSON AGENTS; BENZAZEPINES; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE ANTAGONISTS; EVOKED POTENTIALS; FUNCTIONAL LATERALITY; LEVODOPA; MALE; MOTOR ACTIVITY; OXIDOPAMINE; PARKINSONIAN DISORDERS; RATS; RATS, LONG-EVANS; SUBTHALAMIC NUCLEUS; TIME FACTORS; TYROSINE 3-MONOOXYGENASE; WAKEFULNESS;

EID: 84929378770     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0587-15.2015     Document Type: Article

References (64)

1. Alegre M, Alonso-Frech F, Rodriguez-Oroz MC, Guridi J, Zamarbide I, Valencia M, Manrique M, Obeso JA, Artieda J (2005) Movement-related changes in oscillatory activity in the human subthalamic nucleus: ipsilat-eral vs contralateral movements. Eur J Neurosci 22:2315-2324. CrossRef Medline
2. Alonso-Frech F, Zamarbide I, Alegre M, Rodriguez-Oroz MC, Guridi J, Manrique M, Valencia M, Artieda J, Obeso JA (2006) Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. Brain 129: 1748-1757. CrossRef Medline
3. Anzak A, Gaynor L, Beigi M, Limousin P, Hariz M, Zrinzo L, Foltynie T, Brown P, Jahanshahi M (2011) A gamma band specific role of the subthalamic nucleus in switching during verbal fluency tasks in Parkinson's disease. Exp Neurol 232:136-142. CrossRef Medline
4. Anzak A, Gaynor L, Beigi M, Foltynie T, Limousin P, Zrinzo L, Brown P, Jahanshahi M (2013) Subthalamic nucleus gamma oscillations mediate a switch from automatic to controlled processing: a study of random number generation in Parkinson's disease. Neuroimage 64:284-289. CrossRef Medline
5. Avila I, Parr-Brownlie LC, Brazhnik E, Castaneda E, Bergstrom DA, Walters JR (2010) Beta frequency synchronization in basal ganglia output during rest and walk in a hemiparkinsonian rat. Exp Neurol 221:307-319. CrossRef Medline
6. Baunez C, Lardeux S (2011) Frontal cortex-like functions of the subthalamic nucleus. Front Syst Neurosci 5:83. CrossRef Medline
7. Benchenane K, Tiesinga PH, Battaglia FP (2011) Oscillations in the prefron-tal cortex: a gateway to memory and attention. Curr Opin Neurobiol 21:475-485. CrossRef Medline
8. Berke JD (2009) Fast oscillations in cortical-striatal networks switch frequency following rewarding events and stimulant drugs. Eur J Neurosci 30:848-859. CrossRef Medline
9. Biseul I, Sauleau P, Haegelen C, Trebon P, Drapier D, Raoul S, Drapier S, Lallement F, Rivier I, Lajat Y, Verin M (2005) Fear recognition is impaired by subthalamic nucleus stimulation in Parkinson's disease. Neu-ropsychologia 43:1054-1059. CrossRef Medline
10. Brazhnik E, Cruz AV, Avila I, Wahba MI, Novikov N, Ilieva NM, McCoy AJ, Gerber C, Walters JR (2012) State-dependent spike and local field synchronization between motor cortex and substantia nigra in hemiparkinsonian rats. J Neurosci 32:7869-7880. CrossRef Medline
11. Brazhnik E, Novikov N, McCoy AJ, Cruz AV, Walters JR (2014) Functional correlates of exaggerated oscillatory activity in basal ganglia output in hemiparkinsonian rats. Exp Neurol 261:563-577. CrossRef Medline
12. Brittain JS, Brown P (2014) Oscillations and the basal ganglia: motor control and beyond. Neuroimage 85:637-647. CrossRef Medline
13. Brown P (2003) O scillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov Disord 18:357-363. CrossRef Medline
14. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci 21:1033-1038. Medline
15. Brown P, Kupsch A, Magill PJ, Sharott A, Harnack D, Meissner W (2002) Oscillatory local field potentials recorded from the subthalamic nucleus of the alert rat. Exp Neurol 177:581-585. CrossRef Medline
16. Brücke C, Kempf F, Kupsch A, Schneider GH, Krauss JK, Aziz T, Yarrow K, Pogosyan A, Brown P, Kühn AA (2008) Movement-related synchronization of gamma activity is lateralized in patients with dystonia. Eur J Neurosci 27:2322-2329. CrossRef Medline
17. Brücke C, Bock A, Huebl J, Krauss JK, Schönecker T, Schneider GH, Brown P, Kühn AA (2013) Thalamic gamma oscillations correlate with reaction time in a Go/no Go task in patients with essential tremor. Neuroimage 75:36-45. CrossRef Medline
18. Brunenberg EJ, Moeskops P, Backes WH, Polio C, Cammoun L, Vilanova A, Janssen ML, Visser-Vandewalle VE, ter Haar Romeny BM, Thiran JP, Platel B (2012) Structural and resting state functional connectivity of the subthalamic nucleus: identification of motor STN parts and the hyperdi-rect pathway. PLoS One 7:e39061. CrossRef Medline
19. Carta M, Carlsson T, Kirik D, Björklund A (2007) Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 130:1819-1833. CrossRef Medline
20. Cassidy M, Mazzone P, Oliviero A, Insola A, Tonali P, Di Lazzaro V, Brown P (2002) Movement-related changes in synchronization in the human basal ganglia. Brain 125:1235-1246. CrossRef Medline
21. Castrioto A, Lhommée E, Moro E, Krack P (2014) Mood and behavioural effects of subthalamic stimulation in Parkinson's disease. Lancet Neurol 13:287-305. CrossRef Medline
22. Delaville C, Cruz AV, McCoy AJ, Brazhnik E, Avila I, Novikov N, Walters JR (2014) Oscillatory activity in basal ganglia and motor cortex in an awake behaving rodent model of Parkinson's disease. Basal Ganglia 3:221-227. CrossRef Medline
23. Donnelly NA, Holtzman T, Rich PD, Nevado-Holgado AJ, Fernando AB, Van Dijck G, Holzhammer T, Paul O, Ruther P, Paulsen O, Robbins TW, Dailey JW (2014) Oscillatory activity in the medial prefrontal cortex and nucleus accumbens correlates with impulsivity and reward outcome. PLoS One 9:el 11300. CrossRef Medline
24. Eisenstein SA, Dewispelaere WB, Campbell MC, Lugar HM, Perlmutter JS, Black KJ, Hershey T (2014) Acute changes in mood induced by subthalamic deep brain stimulation in Parkinson disease are modulated by psychiatric diagnosis. Brain Stimul 7:701-708. CrossRef Medline
25. Eusebio A, Brown P (2007) Oscillatory activity in the basal ganglia. Parkinsonism Relat Disord 13:S434-S436. CrossRef Medline
26. Florin E, Erasmi R, Reck C, Maarouf M, Schnitzler A, Fink GR, Timmermann L (2013) Does increased gamma activity in patients suffering from Parkinson's disease counteract the movement inhibiting beta activity? Neuroscience 237:42-50. CrossRef Medline
27. Foffani G, Priori A, Egidi M, Rampini P, Tamma F, Caputo E, Moxon KA, Cerutti S, Barbieri S (2003) 300-Hz subthalamic oscillations in Parkinson's disease. Brain 126:2153-2163. CrossRef Medline
28. Fogelson N, Williams D, Tijssen M, van Bruggen G, Speelman H, Brown P (2006) Different functional loops between cerebral cortex and the sub-thalmic area in Parkinson's disease. Cereb Cortex 16:64-75. CrossRef Medline
29. Friston KJ, Bastos AM, Pinotsis D, Litvak V (2015) LFP and oscillations-what do they tell us? Curr Opin Neurobiol 31:1-6. CrossRef Medline
30. Halje P, Tamtè M, Richter U, Mohammed M, Cenci MA, Petersson P (2012) Levodopa-induced dyskinesia is strongly associated with resonant cortical oscillations. J Neurosci 32:16541-16551. CrossRef Medline
31. Haynes WI, Haber SN (2013) The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for Basal Ganglia models and deep brain stimulation. J Neurosci 33:4804-4814. CrossRef Medline
32. Jahanshahi M, Obeso I, Baunez C, Alegre M, Krack P (2015) Parkinson's disease, the subthalamic nucleus, inhibition, and impulsivity. Mov Disord 30: 128-140. CrossRef Medline
33. Jenkinson N, Brown P (2011) New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci 34: 611-618. CrossRef Medline
34. Jenkinson N, Kühn AA, Brown P (2013) Gamma oscillations in the human basal ganglia. Exp Neurol 245:72-76. CrossRef Medline
35. Joundi RA, Brittain JS, Green AL, Aziz TZ, Brown P, Jenkinson N (2012) Oscillatory activity in the subthalamic nucleus during arm reaching in Parkinson's disease. Exp Neurol 236:319-326. CrossRef Medline
36. Kempf F, Kühn AA, Kupsch A, Brücke C, Weise L, Schneider GH, Brown P (2007) Premovement activities in the subthalamic area of patients with Parkinson's disease and their dependence on task. Eur J Neurosci 25: 3137-3145. CrossRef Medline
37. Kempf F, Brücke C, Salih F, Trottenberg T, Kupsch A, Schneider GH, Doyle Gaynor LM, Hoffmann KT, Vesper J, Wöhrle J, Altenmüller DM, Krauss JK, Mazzone P, Di Lazzaro V, Yelnik J, Kühn AA, Brown P (2009) Gamma activity and reactivity in human thalamic local field potentials. Eur J Neurosci 29:943-953. CrossRef Medline
38. Kolomiets BP, Deniau JM, Mailly P, Ménétrey A, Glowinski J, Thierry AM (2001) Segregation and convergence of information flow through the cortico-subthalamic pathways. J Neurosci 21:5764-5772. Medline
39. Kühn AA, Williams D, Kupsch A, Limousin P, Hariz M, Schneider GH, Yarrow K, Brown P (2004) Event-related beta desynchronization in hu-man subthalamic nucleus correlates with motor performance. Brain 127: 735-746. CrossRef Medline
40. Kühn AA, Trottenberg T, Kivi A, Kupsch A, Schneider GH, Brown P (2005) The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease. Exp Neurol 194:212-220. CrossRef Medline
41. Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain 125:1196-1209. CrossRef Medline
42. Lew SE, Tseng KY (2014) Dopamine modulation of GABAergic function enables network stability and input selectivity for sustaining working memory in a computational model of the prefrontal cortex. Neuropsychopharmacology 39:3067-3076. CrossRef Medline
43. Löpez-Azcarate J, Tainta M, Rodriguez-Oroz MC, Valencia M, González R, Guridi J, Iriarte J, Obeso JA, Artieda J, Alegre M (2010) Coupling between beta and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson's disease. J Neurosci 30:6667-6677. CrossRef Medline
44. Mitra PP, Bokil H (2007) Observed brain dynamics. Oxford UP.
45. Olsson M, Nikkhah G, Bentlage C, Björklund A (1995) Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 15:3863-3875. Medline
46. Oswal A, Brown P, Litvak V (2013) Synchronized neural oscillations and the pathophysiology of Parkinson's disease. Curr Opin Neurol 26:662-670. CrossRef Medline
47. Priori A, Foffani G, Pesenti A, Bianchi A, Chiesa V, Baselli G, Caputo E, Tamma F, Rampini P, Egidi M, Locatelli M, Barbieri S, Scarlato G (2002) Movement-related modulation of neural activity in human basal ganglia and its L-DOPA dependency: recordings from deep brain stimulation electrodes in patients with Parkinson's disease. Neurol Sci 23 [Suppl 2]: S101-S102. CrossRef Medline
48. Priori A, Foffani G, Pesenti A, Tamma F, Bianchi AM, Pellegrini M, Locatelli M, Moxon KA, Villani RM (2004) Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease. Exp Neurol 189:369-379. CrossRef Medline
49. Rektor I, Bocková M, Chrastina J, Rektorova I, Baláž M (2015) The modulatory role of subthalamic nucleus in cognitive functions-A viewpoint. Clin Neurophysiol 126:653-658. CrossRef Medline
50. Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM (1989) The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53:1-31. CrossRef Medline
51. Sharott A, Magill PJ, Harnack D, Kupsch A, Meissner W, Brown P (2005) Dopamine depletion increases the power and coherence of beta-oscillations in the cerebral cortex and subthalamic nucleus of the awake rat. Eur J Neurosci 21:1413-1422. CrossRef Medline
52. Sharott A, Gulberti A, Zittel S, Tudor Jones AA, Fickel U, Münchau A, Köp-pen JA, Gerloff C, Westphal M, Buhmann C, Hamel W, Engel AK, Moll CK (2014) Activity parameters of subthalamic nucleus neurons selectively predict motor symptom severity in Parkinson's disease. J Neurosci 34:6273-6285. CrossRef Medline
53. Stein E, Bar-Gad I (2013) Beta oscillations in the cortico-basal ganglia loop during parkinsonism. Exp Neurol 245:52-59. CrossRef Medline
54. Tan H, Pogosyan A, Anzak A, Ashkan K, Bogdanovic M, Green AL, Aziz T, Foltynie T, Limousin P, Zrinzo L, Brown P (2013) Complementary roles of different oscillatory activities in the subthalamic nucleus in coding motor effort in Parkinsonism. Exp Neurol 248:187-195. CrossRef Medline
55. Tan SK, Temel Y, Blokland A, Steinbusch HW, Visser-Vandewalle V (2006) The subthalamic nucleus: from response selection to execution. J Chem Neuroanat 31:155-161. CrossRef Medline
56. Temel Y, Kessels A, Tan S, Topdag A, Boon P, Visser-Vandewalle V (2006) Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat Disord 12: 265-272. CrossRef Medline
57. Trottenberg T, Fogelson N, Kühn AA, Kivi A, Kupsch A, Schneider GH, Brown P (2006) Subthalamic gamma activity in patients with Parkinson's disease. Exp Neurol 200:56-65. CrossRef Medline
58. van der Meer MA, Redish AD (2009) Low and high gamma oscillations in rat ventral striatum have distinct relationships to behavior, reward, and spiking activity on a learned spatial decision task. Front Integr Neurosci 3:9. CrossRef Medline
59. van der Meer MA, Kalenscher T, Lansink CS, Pennartz CM, Berke JD, Redish AD (2010) Integrating early results on ventral striatal gamma oscillations in the rat. Front Neurosci 4:300. CrossRef Medline
60. Weinberger M, Mahant N, Hutchison WD, Lozano AM, Moro E, Hodaie M, Lang AE, Dostrovsky JO (2006) Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease. J Neurophysiol 96:3248-3256. CrossRef Medline
61. Weinberger M, Hutchison WD, Lozano AM, Hodaie M, Dostrovsky JO (2009) Increased gamma oscillatory activity in the subthalamic nucleus during tremor in Parkinson's disease patients. J Neurophysiol 101:789-802. CrossRef Medline
62. Williams D, Tijssen M, Van Bruggen G, Bosch A, Insola A, Di Lazzaro V, Mazzone P, Oliviero A, Quartarone A, Speelman H, Brown P (2002) Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 125:1558-1569. CrossRef Medline
63. Womelsdorf T, Fries P (2007) The role of neuronal synchronization in selective attention. Curr Opin Neurobiol 17:154-160. CrossRef Medline
64. Yang AI, Vanegas N, Lungu C, Zaghloul KA (2014) Beta-coupled high-frequency activity and beta-locked neuronal spiking in the subthalamic nucleus of Parkinson's disease. J Neurosci 34:12816-12827. CrossRef Medline