Central thalamic deep-brain stimulation alters striatal-thalamic connectivity in cognitive neural behavior

Frontiers in Neural Circuits

Volumn 9, Issue JAN2016, 2016, Pages

  Lin, Hui Ching ^a   Pan, Han Chi ^a   Lin, Sheng Huang ^b,c   Lo, Yu Chun ^d   Shen, Elise Ting Hsin ^c   Liao, Lun De ^e,f   Liao, Pei Han ^a   Chien, Yi Wei ^a   Liao, Kuei Da ^c   Jaw, Fu Shan ^c   Chu, Kai Wen ^a   Lai, Hsin Yi ^g   Chen, You Yin ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TZU CHI UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^g ZHEJIANG UNIVERSITY   (China)

Author keywords

Deep brain stimulation; Functional connectivity; Local field potentials; Reward associated learning; Thalamus

Indexed keywords

CHOLINERGIC RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE RECEPTOR; NICOTINIC RECEPTOR ALPHA4; PROTEIN C FOS; DRD2 PROTEIN, RAT; NICOTINIC ACETYLCHOLINE RECEPTOR ALPHA4 SUBUNIT; NICOTINIC RECEPTOR;

ADULT; ALPHA RHYTHM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA RHYTHM; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CENTRAL THALAMIC DEEP BRAIN STIMULATION; CHOLINERGIC SYSTEM; COGNITION; CONNECTOME; CONTROLLED STUDY; CORPUS STRIATUM; DELTA RHYTHM; DOPAMINERGIC SYSTEM; MALE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; OSCILLATION; PROTEIN EXPRESSION; RAT; THALAMUS; THALAMUS LATERAL NUCLEUS; THETA RHYTHM; ANIMAL; HEMISPHERIC DOMINANCE; HIPPOCAMPUS; LEARNING; METABOLISM; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; PROCEDURES; REWARD; SPRAGUE DAWLEY RAT;

ALPHA RHYTHM; ANIMALS; COGNITION; CORPUS STRIATUM; DEEP BRAIN STIMULATION; FUNCTIONAL LATERALITY; HIPPOCAMPUS; LEARNING; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PROTO-ONCOGENE PROTEINS C-FOS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D2; RECEPTORS, NICOTINIC; REWARD; THALAMUS; THETA RHYTHM;

EID: 84957880662     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2015.00087     Document Type: Article

References (68)

1. Atallah, H. E., Lopez-Paniagua, D., Rudy, J. W., and O’Reilly, R. C. (2007). Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nat. Neurosci. 10, 126-131. doi: 10.1038/nn1817
2. Baik, J. H., Picetti, R., Saiardi, A., Thiriet, G., Dierich, A., Depaulis, A., Borrelli, E. (1995). Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors. Nature 377, 424-428. doi: 10.1038/377424a0
3. Baizabal Carvallo, J. F., Simpson, R., and Jankovic, J. (2011). Diagnosis and treatment of complications related to deep brain stimulation hardware. Mov. Disord. 26, 1398-1406. doi: 10.1002/mds.23800
4. Balleine, B. W., Killcross, A. S., and Dickinson, A. (2003). The effect oflesions ofthe basolateral amygdala on instrumental conditioning. J. Neurosci. 23, 666-675.
5. Basar, E., Basar-Eroglu, C., Karakas, S., and Schurmann, M. (2001). Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int. J. Psychophysiol. 39, 241-248. doi: 10.1016/S0167-8760(00)00145-8
6. Bergman, H., Feingold, A., Nini, A., Raz, A., Slovin, H., Abeles, M., et al. (1998). Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 21, 32-38.
7. Bush, G., Luu, P., and Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215-222. doi: 10.1016/S1364-6613(00)01483-2
8. Buzsaki, G. (2002). Theta oscillations in the hippocampus. Neuron 33, 325-340. doi: 10.1016/S0896-6273(02)00586-X
9. Calabresi, P., and Di Filippo, M. (2008). ACh/dopamine crosstalk in motor control and reward: a crucial role for alpha 6-containing nicotinic receptors? Neuron 60,4-7. doi: 10.1016/j.neuron.2008.09.031
10. Calabresi, P., Picconi, B., Parnetti, L., and Di Filippo, M. (2006). A convergent model for cognitive dysfunctions in Parkinson’s disease: the critical dopamineacetylcholine synaptic balance. Lancet Neurol. 5, 974-983. doi: 10.1016/S1474-4422(06)70600-7
11. Cardinal, R. N., and Cheung, T. H. C. (2005). Nucleus accumbens core lesions retard instrumental learning and performance with delayed reinforcement in the rat. BMC Neurosci. 6:9. doi: 10.1186/1471-2202-6-9
12. Chen, C. H., Fremont, R., Arteaga-Bracho, E. E., and Khodakhah, K. (2014). Short latency cerebellar modulation of the basal ganglia. Nat. Neurosci. 17, 1767-1775. doi: 10.1038/nn.3868
13. Cragg, S. J. (2006). Meaningful silences: how dopamine listens to the ACh pause. Trends Neurosci. 29, 125-131. doi: 10.1016/j.tins.2006.01.003
14. Deschenes, M., Bourassa, J., and Parent, A. (1996). Striatal and cortical projections of single neurons from the central lateral thalamic nucleus in the rat. Neuroscience 72, 679-687.
15. Deuschl, G., Raethjen, J., Lindemann, M., and Krack, P. (2001). The pathophysiology of tremor. MuscleNerve 24, 716-735. doi: 10.1002/mus.1063
16. Eddy, M. C., Stansfield, K. J., and Green, J. T. (2014). Voluntary exercise improves performance of a discrimination task through effects on the striatal dopamine system. Learn. Mem. 21, 334-337. doi: 10.1101/lm.034462.114
17. Ego-Stengel, V., and Wilson, M. A. (2010). Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20, 1-10. doi: 10.1002/hipo.20707
18. Fell, J., Staresina, B. P., Do Lam, A. T., Widman, G., Helmstaedter, C., Elger, C. E., et al. (2013). Memorymodulation byweak synchronous deepbrain stimulation: a pilot study. Brain Stimul. 6, 270-273. doi: 10.1016/j.brs.2012.08.001
19. Flora, E. D., Perera, C. L., Cameron, A. L., and Maddern, G. J. (2010). Deep brain stimulation for essential tremor: a systematic review. Mov. Disord. 25, 1550-1559. doi: 10.1002/mds.23195
20. Fries, P. (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474-480. doi: 10.1016/j.tics.2005.08.011
21. Halgren, E., Wilson, C. L., and Stapleton, J. M. (1985). Human medial temporal- lobe stimulation disrupts both formation and retrieval of recent memories. Brain Cogn. 4, 287-295. doi: 10.1016/0278-2626(85)90022-3
22. Hasselmo, M. E., Hay, J., Ilyn, M., and Gorchetchnikov, A. (2002). Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw. 15, 689-707. doi: 10.1016/S0893-6080(02)00057-6
23. Ishii, R., Shinosaki, K., Ukai, S., Inouye, T., Ishihara, T., Yoshimine, T., et al. (1999). Medial prefrontal cortex generates frontal midline theta rhythm. Neuroreport 10, 675-679.
24. Jacquet, M., Lecourtier, L., Cassel, R., Loureiro, M., Cosquer, B., Escoffier, G., et al. (2013). Dorsolateral striatum and dorsal hippocampus: a serial contribution to acquisition of cue-reward associations in rats. Behav. Brain Res. 239, 94-103. doi: 10.1016/j.bbr.2012.10.061
25. Jones, E. G. (2009). Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. Ann. N. Y. Acad. Sci. 1157, 10-23. doi: 10.1111/j.1749-6632.2009.04534.x
26. Kesner, R. P. (2013). A process analysis of the CA3 subregion of the hippocampus. Front. Cell. Neurosci. 7:78. doi: 10.3389/fncel.2013.00078
27. Kirov, R., Weiss, C., Siebner, H. R., Born, J., and Marshall, L. (2009). Slow oscillation electrical brain stimulation during waking promotes EEG theta activityand memoryencoding. Proc. Natl. Acad. Sci. U.S.A. 106, 15460-15465. doi: 10.1073/pnas.0904438106
28. Klimesch, W., Doppelmayr, M., Pachinger, T., and Ripper, B. (1997). Brain oscillations and human memory: EEG correlates in the upper alpha and theta band. Neurosci. Lett. 238, 9-12.
29. Knyazev, G. G. (2007). Motivation, emotion, and their inhibitory control mirrored in brain oscillations. Neurosci. Biobehav. Rev. 31, 377-395. doi: 10.1016/j.neubiorev.2006.10.004
30. Kolb, B., Sutherland, R. J., and Whishaw, I. Q. (1983). A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. Behav. Neurosci. 97, 13-27.
31. Labarca, C., Schwarz, J., Deshpande, P., Schwarz, S., Nowak, M. W., Fonck, C., et al. (2001). Point mutant mice with hypersensitive alpha 4 nicotinic receptors show dopaminergic deficits and increased anxiety. Proc. Natl. Acad. Sci. U.S.A. 98, 2786-2791. doi: 10.1073/pnas.041582598
32. Lacruz, M. E., Valentin, A., Seoane, J. J. G., Morris, R. G., Selway, R. P., and Alarcon, G. (2010). Single pulse electrical stimulation of the hippocampus is sufficient to impair human episodic memory. Neuroscience 170, 623-632. doi: 10.1016/j.neuroscience.2010.06.042
33. Lee, H., Fell, J., and Axmacher, N. (2013). Electrical engram: how deep brain stimulation affects memory. Trends Cogn. Sci. 17, 574-584. doi: 10.1016/j.tics.2013.09.002
34. Lepski, G., Arevalo, A., do Valle, A. C., Ballester, G., and Gharabaghi, A. (2012). Increased coherence among striatal regions in the theta range during attentive wakefulness. Braz. J. Med. Biol. Res. 45, 763-770. doi: 10.1590/S0100-879X2012007500104
35. Leung, L. S., and Shen, B. (2006). Hippocampal CA1 kindling but not long-term potentiation disrupts spatial memoryperformance. Learn. Mem. 13,18-26. doi: 10.1101/lm.66106
36. Levin, E. D., and Simon, B. B. (1998). Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology (Berl) 138, 217-230.
37. Luciana, M., Depue, R. A., Arbisi, P., and Leon, A. (1992). Facilitation of working memory in humans by a d2 dopamine receptor agonist. J. Cogn. Neurosci. 4, 58-68. doi: 10.1162/jocn.1992.4.1.58
38. Maguire, E. A. (2001). The retrosplenial contribution to human navigation: a review oflesion and neuroimaging findings. Scand. J. Psychol. 42, 225-238. doi: 10.1111/1467-9450.00233
39. McCracken, C. B., and Grace, A. A. (2009). Nucleus accumbens deep brain stimulation produces region-specific alterations in local field potential oscillations and evoked responses in vivo. J. Neurosci. 29, 5354-5363. doi: 10.1523/JNEUROSCI.0131-09.2009
40. Mengual, E., de las Heras, S., Erro, E., Lanciego, J. L., and Gimenez-Amaya, J. M. (1999). Thalamic interaction between the input and the output systems of the basal ganglia. J. Chem. Neuroanat. 16, 187-200. doi: 10.1016/S0891-0618(99)00010-1
41. Nagel, S. J., Machado, A. G., Gale, J. T., Lobel, D. A., and Pandya, M. (2015). Preserving cortico-striatal function: deep brain stimulation in Huntington’s disease. Front. Syst. Neurosci. 9:32. doi: 10.3389/fnsys.2015.00032
42. Neale, C., Johnston, P., Hughes, M., and Scholey, A. (2015). Functional activation during the rapid visual information processing task in a middle aged cohort: an fMRI study. PLoS ONE 10:e0138994. doi: 10.1371/journal.pone.0138994
43. Overbeek, J. M., de Koning, P., Luigjes, J., van den Munckhof, P., Schuurman, P. R., and Denys, D. (2013). Deep brain stimulation for psychiatric disorders. Ned. Tjdschr. Geneeskd. 157, A7015.
44. Parikh, V., and Sarter, M. (2008). Cholinergic mediation of attention: contributions ofphasic and tonic increases in prefrontal cholinergic activity. Ann. N. Y. Acad. Sci. 1129, 225-235. doi: 10.1196/annals.1417.021
45. Paxinos, G., and Watson, C. (2005). The Rat Brain in Sterotaxic Coordinates. Amsterdam; Boston, MA: Elsevier Academic Press.
46. Ragozzino, M. E., and Rozman, S. (2007). The effect of rat anterior cingulate inactivation on cognitive flexibility. Behav. Neurosci. 121, 698-706. doi: 10.1037/0735-7044.121.4.698
47. Robbins, T. W., and Arnsten, A. F. (2009). The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu. Rev. Neurosci. 32, 267-287. doi: 10.1146/annurev.neuro.051508.135535
48. Ross, S. A., Wong, J. Y., Clifford, J. J., Kinsella, A., Massalas, J. S., Horne, M. K., et al. (2000). Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J. Neurosci. 20, 6431-6441.
49. Schiff, N. D., Giacino, J. T., Kalmar, K., Victor, J. D., Baker, K., Gerber, M., et al. (2007). Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600-603. doi: 10.1038/nature06041
50. Schlaepfer, T. E., and Bewernick, B. H. (2014). Neuromodulation for treatment resistant depression: state of the art and recommendations for clinical and scientific conduct. Brain Topogr. 27, 12-19. doi: 10.1007/s10548-013-0315-9
51. Shirvalkar, P., Seth, M., Schiff, N. D., and Herrera, D. G. (2006). Cognitive enhancementwith central thalamic electrical stimulation. Proc. Natl. Acad. Sci. U.S.A. 103, 17007-17012. doi: 10.1073/pnas.0604811103
52. Skinner, B. F. (1992). ‘Superstition' in the pigeon. 1948. J. Exp. Psychol. Gen. 121, 273-274.
53. Squire, L. R., Stark, C. E., and Clark, R. E. (2004). The medial temporal lobe. Annu. Rev. Neurosci. 27, 279-306. doi: 10.1146/annurev.neuro.27.070203.144130
54. Srinath, R., and Ray, S. (2014). Effect of amplitude correlations on coherence in the local fieldpotential. J.Neurophysiol. 112,741-751. doi: 10.1152/jn.00851.2013
55. Stone, S. S., Teixeira, C. M., Devito, L. M., Zaslavsky, K., Josselyn, S. A., Lozano, A. M., et al. (2011). Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J. Neurosci. 31, 13469-13484. doi: 10.1523/JNEUR0SCI.3100-11.2011
56. Sturman, D. A., and Moghaddam, B. (2011). Reduced neuronal inhibition and coordination of adolescent prefrontal cortex during motivated behavior. J. Neurosci. 31, 1471-1478. doi: 10.1523/JNEUR0SCI.4210-10.2011
57. Suthana, N., and Fried, I. (2014). Deep brain stimulation for enhancement of learning and memory. Neuroimage 85(Pt 3), 996-1002. doi: 10.1016/j.neuroimage.2013.07.066
58. Suthana, N., Haneef, Z., Stern, J., Mukamel, R., Behnke, E., Knowlton, B., et al. (2012). Memory enhancement and deep-brain stimulation of the entorhinal area. N. Engl.J. Med. 366, 502-510. doi: 10.1056/NEJMoa1107212
59. Thorn, C. A., and Graybiel, A. M. (2014). Differential entrainment and learning-related dynamics of spike and local field potential activity in the sensorimotor and associative striatum. J. Neurosci. 34, 2845-2859. doi: 10.1523/JNEUR0SCI.1782-13.2014
60. Tort, A. B., Kramer, M. A., Thorn, C., Gibson, D. J., Kubota, Y., Graybiel, A. M., et al. (2008). Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc. Natl. Acad. Sci. U.S.A. 105, 20517-20522. doi: 10.1073/pnas.0810524105
61. Vann, S. D., Aggleton, J. P., and Maguire, E. A. (2009). What does the retrosplenial cortex do? Nat. Rev. Neurosci. 10, 792-802. doi: 10.1038/nrn2733
62. Vitek, J. L., and Giroux, M. (2000). Physiology of hypokinetic and hyperkinetic movement disorders: model for dyskinesia. Ann. Neurol. 47(4 Suppl. 1), S131-S140.
63. Wang, M., Vijayraghavan, S., and Goldman-Rakic, P. S. (2004). Selective D2 receptor actions on the functional circuitry of working memory. Science 303, 853-856. doi: 10.1126/science.1091162
64. Waters, N. S., Klintsova, A. Y., and Foster, T. C. (1997). Insensitivity of the hippocampus to environmental stimulation during postnatal development. J. Neurosci. 17, 7967-7973.
65. Williams, N. R., and Okun, M. S. (2013). Deep brain stimulation (DBS) at the interface of neurology and psychiatry. J. Clin. Invest. 123, 4546-4556. doi: 10.1172/JCI68341
66. Womelsdorf, T., Vinck, M., Leung, L. S., and Everling, S. (2010). Selective theta-synchronization of choice-relevant information subserves goal-directed behavior. Front. Hum. Neurosci. 4:210. doi: 10.3389/fnhum.2010.00210
67. Yin, H. H., and Knowlton, B. J. (2006). The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464-476. doi: 10.1038/nrn1919
68. Yin, H. H., Ostlund, S. B., and Balleine, B. W. (2008). Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur. J. Neurosci. 28, 1437-1448. doi: 10.1111/j.1460-9568.2008.06422.x