Selective effects of dopamine depletion and L-DOPA therapy on learning-related firing dynamics of striatal neurons

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 4782-4795

  Hernandez, Ledia F ^a   Kubota, Yasuo ^a   Hu, Dan ^a   Howe, Mark W ^a   Lemaire, Nuné ^a   Graybiel, Ann M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; LEVODOPA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONDITIONED REFLEX; CONTROLLED STUDY; CORPUS STRIATUM; CYCLIC POTENTIOMETRY; DATA ANALYSIS; HISTOLOGY; INTERNEURON; LEARNING; MALE; MAZE TEST; NERVE CONDUCTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; REACTION TIME; SENSORIMOTOR FUNCTION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CONDITIONING, OPERANT; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE AGENTS; ELECTRIC STIMULATION; ELECTROCHEMICAL TECHNIQUES; LEARNING DISORDERS; LEVODOPA; MALE; MAZE LEARNING; NEURAL PATHWAYS; NEUROTOXINS; OXIDOPAMINE; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; TIME FACTORS;

EID: 84874825985     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3746-12.2013     Document Type: Article

References (43)

1. Andreu N, Chalé JJ, Senard JM, Thalamas C, Montastruc JL, Rascol O (1999) L-Dopa-induced sedation: a double-blind cross-over controlled study versus triazolam and placebo in healthy volunteers. Clin Neuropharmacol 22:15-23. CrossRef Medline
2. Aosaki T, Graybiel AM, Kimura M (1994a) Effects of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265:412-415. CrossRef Medline
3. Aosaki T, Tsubokawa H, Ishida A, Watanabe K, Graybiel AM, Kimura M (1994b) Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14:3969-3984. Medline
4. Apicella P (2007) Leading tonically active neurons of the striatum from reward detection to context recognition. Trends Neurosci 30:299-306. CrossRef Medline
5. Barnes TD, Mao JB, Hu D, Kubota Y, Dreyer AA, Stamoulis C, Brown EN, Graybiel AM (2011) Advance cueing produces enhanced actionboundary patterns of spike activity in the sensorimotor striatum. J Neurophysiol 105:1861-1878. CrossRef Medline
6. Barnes TD, Kubota Y, Hu D, Jin DZ, Graybiel AM (2005) Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437:1158-1161. CrossRef Medline
7. Bennett BD, Bolam JP (1994) Synaptic input and output of parvalbuminimmunoreactive neurons in the neostriatum of the rat. Neuroscience 62:707-719. CrossRef Medline
8. Berke JD (2011) Functional properties of striatal fast-spiking interneurons. Front Syst Neurosci 5:45. Medline
9. Braak H, Braak E (2000) Pathoanatomy of Parkinson's disease. J Neurol 247 [Suppl 2]:II3-10. Medline
10. Brown P (2007) Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Curr Opin Neurobiol 17:656-664. CrossRef Medline
11. Calabresi P, Mercuri NB, Sancesario G, Bernardi G (1993) Electrophysiology of dopamine-denervated striatal neurons. Implications for Parkinson's disease. Brain 116:433-452. CrossRef Medline
12. Cameron IG, Watanabe M, Pari G, Munoz DP (2010) Executive impairment in Parkinson's disease: response automaticity and task switching. Neuropsychologia 48:1948-1957. CrossRef Medline
13. Centonze D, Gubellini P, Picconi B, Calabresi P, Giacomini P, Bernardi G (1999) Unilateral dopamine denervation blocks corticostriatal LTP. J Neurophysiol 82:3575-3579. Medline
14. Chen MT, Morales M, Woodward DJ, Hoffer BJ, Janak PH (2001) In vivo extracellular recording of striatal neurons in the awake rat following unilateral 6-hydroxydopamine lesions. Exp Neurol 171:72-83. CrossRef Medline
15. Clark JJ, Sandberg SG, Wanat MJ, Gan JO, Horne EA, Hart AS, Akers CA, Parker JG, Willuhn I, Martinez V, Evans SB, Stella N, Phillips PE (2010) Chronic microsensors for longitudinal, subsecond dopamine detection in behaving animals. Nat Methods 7:126-129. CrossRef Medline
16. Cools R, Barker RA, Sahakian BJ, Robbins TW (2001) Mechanisms of cognitive set flexibility in Parkinson's disease. Brain 124:2503-2512. CrossRef Medline
17. Day M, Wang Z, Ding J, An X, Ingham CA, Shering AF, Wokosin D, Ilijic E, Sun Z, Sampson AR, Mugnaini E, Deutch AY, Sesack SR, Arbuthnott GW, Surmeier DJ (2006) Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 9:251-259. CrossRef Medline
18. Emondi AA, Rebrik SP, Kurgansky AV, Miller KD (2004) Tracking neurons recorded from tetrodes across time. J Neurosci Methods 135:95-105. CrossRef Medline
19. Faure A, Haberland U, Condé F, El Massioui N (2005) Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J Neurosci 25:2771-2780. CrossRef Medline
20. Gerfen CR, Surmeier DJ (2011) Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34:441-466. CrossRef Medline
21. Gittis AH, Hang GB, LaDow ES, Shoenfeld LR, Atallah BV, Finkbeiner S, Kreitzer AC (2011) Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 71:858-868. CrossRef Medline
22. Goldberg JA, Reynolds JN (2011) Spontaneous firing and evoked pauses in the tonically active cholinergic interneurons of the striatum. Neuroscience 198:27-43. CrossRef Medline
23. Henderson JM, Carpenter K, Cartwright H, Halliday GM (2000) Degeneration of the centre median-parafascicular complex in Parkinson's disease. Ann Neurol 47:345-352. CrossRef Medline
24. Howe MW, Atallah HE, McCool A, Gibson DJ, Graybiel AM (2011) Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum. Proc Natl Acad Sci U S A 108:16801-16806. CrossRef Medline
25. Ingham CA, Hood SH, Arbuthnott GW (1989) Spine density on neostriatal neurones changes with 6-hydroxydopamine lesions and with age. Brain Res 503:334-338. CrossRef Medline
26. Jin X, Costa RM (2010) Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466:457-462. CrossRef Medline
27. Jog MS, Connolly CI, Kubota Y, Iyengar DR, Garrido L, Harlan R, Graybiel AM (2002) Tetrode technology: advances in implantable hardware, neuroimaging, and data analysis techniques. J Neurosci Methods 117: 141-152. CrossRef Medline
28. Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM (1999) Building neural representations of habits. Science 286:1745-1749. CrossRef Medline
29. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923. Medline
30. Keller RW Jr, Kuhr WG, Wightman RM, Zigmond MJ (1988) The effect of L-dopa on in vivo dopamine release from nigrostriatal bundle neurons. Brain Res 447:191-194. CrossRef Medline
31. Kubota Y, Liu J, Hu D, DeCoteau WE, Eden UT, Smith AC, Graybiel AM (2009) Stable encoding of task structure coexists with flexible coding of task events in sensorimotor striatum. J Neurophysiol 102:2142-2160. CrossRef Medline
32. Lacey CJ, Bolam JP, Magill PJ (2007) Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci 27:4374-4384. CrossRef Medline
33. Lansink CS, Goltstein PM, Lankelma JV, Pennartz CM (2010) Fast-spiking interneurons of the rat ventral striatum: temporal coordination of activity with principal cells and responsiveness to reward. Eur J Neurosci 32:494-508. CrossRef Medline
34. Lemaire N, Hernandez LF, Hu D, Kubota Y, Howe MW, Graybiel AM (2012) Effects of dopamine depletion on LFP oscillations in striatum are taskand learning-dependent and selectively reversed by L-DOPA. Proc Natl Acad Sci U S A 109:18126-18131. CrossRef Medline
35. Mallet N, Ballion B, Le Moine C, Gonon F (2006) Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci 26:3875-3884. CrossRef Medline
36. Parthasarathy HB, Graybiel AM (1997) Cortically driven immediate-early gene expression reflects modular influence of sensorimotor cortex on identified striatal neurons in the squirrel monkey. J Neurosci 17:2477-2491. Medline
37. Picconi B, Piccoli G, Calabresi P (2012) Synaptic dysfunction in Parkinson's disease. Adv Exp Med Biol 970:553-572. CrossRef Medline
38. Rice ME, Cragg SJ (2008) Dopamine spillover after quantal release: rethinking dopamine transmission in the nigrostriatal pathway. Brain Res Rev 58:303-313. CrossRef Medline
39. Salin P, López IP, Kachidian P, Barroso-Chinea P, Rico AJ, Gómez-Bautista V, Coulon P, Kerkerian-Le Goff L, Lanciego JL (2009) Changes to interneuron-driven striatal microcircuits in a rat model of Parkinson's disease. Neurobiol Dis 34:545-552. CrossRef Medline
40. Schultz W (2007) Multiple dopamine functions at different time courses. Annu Rev Neurosci 30:259-288. CrossRef Medline
41. Stalnaker TA, Calhoon GG, Ogawa M, Roesch MR, Schoenbaum G (2012) Reward prediction error signaling in posterior dorsomedial striatum is action specific. J Neurosci 32:10296-10305. CrossRef Medline
42. Thorn CA, Atallah H, Howe M, Graybiel AM (2010) Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 66:781-795. CrossRef Medline
43. Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ (2012) Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75:58-64. CrossRef Medline