Delta-frequency stimulation of cerebellar projections can compensate for schizophrenia-related medial frontal dysfunction

Molecular Psychiatry

Volumn 22, Issue 5, 2017, Pages 647-655

  Parker, K L ^a   Kim, Y C ^a   Kelley, R M ^a   Nessler, A J ^a   Chen, K H ^b   Muller Ewald, V A ^c   Andreasen, N C ^a   Narayanan, N S ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Iowa   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; BRAIN NERVE CELL; CEREBELLUM; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; DELTA RHYTHM; FEMALE; HUMAN; MALE; MEDIAL FRONTAL CORTEX; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; SCHIZOPHRENIA; AGED; ANIMAL; CASE CONTROL STUDY; DISEASE MODEL; ELECTROENCEPHALOGRAPHY; FRONTAL LOBE; LONG EVANS RAT; MIDDLE AGED; NERVE CELL; NERVE TRACT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; THALAMUS; TRANSCRANIAL DIRECT CURRENT STIMULATION;

ADULT; AGED; ANIMALS; CASE-CONTROL STUDIES; CEREBELLUM; COGNITION; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; FEMALE; FRONTAL LOBE; HUMANS; MALE; MIDDLE AGED; NEURAL PATHWAYS; NEURONS; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; SCHIZOPHRENIA; THALAMUS; TRANSCRANIAL DIRECT CURRENT STIMULATION;

EID: 85016126650     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2017.50     Document Type: Review

References (54)

1. Andreasen NC, O'Leary DS, Flaum M, Nopoulos P, Watkins GL, Boles Ponto LL et al. Hypofrontality in schizophrenia: distributed dysfunctional circuits in neurolepticnaïve patients. Lancet 1997;349:1730-1734.
2. Goldman-Rakic PS, Castner SA, Svensson TH, Siever LJ, Williams GV. Targeting the dopamine D1 receptor in schizophrenia: insights for cognitive dysfunction. Psychopharmacology (Berl) 2004;174:3-16.
3. Weinberger DR, Berman KF, Zec RF. Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Arch Gen Psychiatry 1986;43:114-124.
4. Parker KL, Narayanan NS, Andreasen NC. The therapeutic potential of the cerebellum in schizophrenia. Front Syst Neurosci 2014;8:163.
5. Parker KL. Timing tasks synchronize cerebellar and frontal ramping activity and theta oscillations: implications for cerebellar stimulation in diseases of impaired cognition. Front Psychiatry 2016;6:190.
6. Buckner RL. The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron 2013;80:807-815.
7. Keren-Happuch E, Chen S-HA, Ho M-HR, Desmond JE. A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp 2012;35593-615.
8. Koziol LF, Budding D, Andreasen N, D'Arrigo S, Bulgheroni S, Imamizu H et al. Consensus Paper: the cerebellum's role in movement and cognition. Cerebellum 2013;13:151-177.
9. Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 2011;11:352-365.
10. Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci 2001;21:700-712.
11. Liu H, Fan G, Xu K, Wang F. Changes in cerebellar functional connectivity and anatomical connectivity in schizophrenia: a combined resting-state functional MRI and diffusion tensor imaging study. J Magn Reson Imag 2011;34:1430-1438.
12. Demirtas-Tatlidede A, Freitas C, Cromer JR, Safar L, Ongur D, Stone WS et al. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr Res 2010;124:91-100.
13. Garg S, Sinha VK, Tikka SK, Mishra P, Goyal N. The efficacy of cerebellar vermal deep high frequency (theta range) repetitive transcranial magnetic stimulation (rTMS) in schizophrenia: a randomized rater blind-sham controlled study. Psychiatry Res 2016;243:413-420.
14. Mittleman G, Goldowitz D, Heck DH, Blaha CD. Cerebellar modulation of frontal cortex dopamine efflux in mice: Relevance to autism and schizophrenia. Synapse 2008;62:544-550.
15. Clausen J. An evaluation of experimental methods of time judgment. J Exp Psychol 1950;40:756-761.
16. Ward RD, Kellendonk C, Kandel ER, Balsam PD. Timing as a window on cognition in schizophrenia. Neuropharmacology 2012;62:1175-1181.
17. Penney TB, Meck WH, Roberts SA, Gibbon J, Erlenmeyer-Kimling L. Interval-timing deficits in individuals at high risk for schizophrenia. Brain Cogn 2005;58:109-118.
18. Ivry RB, Keele SW, Diener HC. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res 1988;73:167-180.
19. Merchant H, Harrington DL, Meck WH. Neural basis of the perception and estimation of time. Annu Rev Neurosci 2013;36:313-336.
20. Parker KL, Chen K-H, Kingyon JR, Cavanagh JF, Narayanan NS. D1-dependent 4 Hz oscillations and ramping activity in rodent medial frontal cortex during interval timing. J Neurosci 2014;34:16774-16783.
21. Laubach M. A comparative perspective on executive and motivational control by the medial prefrontal cortex. In: Mars RB, Sallet J, Rushworth MFS and Yeung N (eds). Neural Basis of Motivational and Cognitive Control. MIT Press: Cambridge, MA, 2011.
22. Parker KL, Chen K-H, Kingyon JR, Cavanagh JF, Naryanan NS. Medial frontal ~ 4 Hz activity in humans and rodents is attenuated in PD patients and in rodents with cortical dopamine depletion. J Neurophysiol 2015;114:1310-1320.
23. Narayanan NS, Cavanagh JF, Frank MJ, Laubach M. Common medial frontal mechanisms of adaptive control in humans and rodents. Nat Neurosci 2013;16:1888-1897.
24. Parker KL, Ruggiero RN, Narayanan NS. Infusion of D1 dopamine receptor agonist into medial frontal cortex disrupts neural correlates of interval timing. Front Behav Neurosci 2015;9:294.
25. Miller BT, D'Esposito M. Searching for 'the top' in top-down control. Neuron 2005;48:535-538.
26. Buschman TJ, Miller EK. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 2007;315:1860-1862.
27. Narayanan NS, Laubach M. Top-down control of motor cortex ensembles by dorsomedial prefrontal cortex. Neuron 2006;52:921-931.
28. Abi-Dargham A, Mawlawi O, Lombardo I, Gil R, Martinez D, Huang Y et al. Prefrontal dopamine D1 receptors and working memory in schizophrenia. J Neurosci 2002;22:3708-3719.
29. Okubo Y, Suhara T, Suzuki K, Kobayashi K, Inoue O, Terasaki O et al. Decreased prefrontal dopamine D1 receptors in schizophrenia revealed by PET. Nature 1997;385:634-636.
30. Fry W, Kelleher RT, Cook L. A mathematical index of performance on fixed-interval schedules of reinforcement. J Exp Anal Behav 1960;3:193-199.
31. Narayanan NS, Land BB, Solder JE, Deisseroth K, DiLeone RJ. Prefrontal D1 dopamine signaling is required for temporal control. Proc Natl Acad Sci USA 2012;109:20726-20731.
32. Barnett L, Seth AK. The MVGC multivariate Granger causality toolbox: a new approach to Granger-causal inference. J Neurosci Methods 2014;223:50-68.
33. Parker KL, Chen K-H, Kingyon JR, Cavanagh JF, Naryanan NS. Medial frontal ~ 4 Hz activity in humans and rodents is attenuated in PD patients and in rodents with cortical dopamine depletion. J Neurophysiol 2015;114:1310-1320.
34. Ward RD, Kellendonk C, Kandel ER, Balsam PD. Timing as a window on cognition in schizophrenia. Neuropharmacology 2011;62:1175-1181.
35. Elvevåg B, McCormack T, Gilbert A, Brown GDA, Weinberger DR, Goldberg TE. Duration judgements in patients with schizophrenia. Psychol Med 2003;33:1249-1261.
36. Ivry RB, Spencer RM. The neural representation of time. Curr Opin Neurobiol 2004;14:225-232.
37. Kim J, Jung AH, Byun J, Jo S, Jung MW. Inactivation of medial prefrontal cortex impairs time interval discrimination in rats. Front Behav Neurosci 2009;3:38.
38. Narayanan NS, Land BB, Solder JE, Deisseroth K, Dileone RJ. Prefrontal D1 dopamine signaling is required for temporal control. Proc Natl Acad Sci USA 2012;109:20726-20731.
39. Narayanan NS. Ramping activity is a cortical mechanism of temporal control of action. Curr Opin Behav Sci 2016;8:226-230.
40. Kim J, Ghim J-W, Lee JH, Jung MW. Neural correlates of interval timing in rodent prefrontal cortex. J Neurosci 2013;33:13834-13847.
41. Xu M, Zhang S, Dan Y, Poo M. Representation of interval timing by temporally scalable firing patterns in rat prefrontal cortex. Proc Natl Acad Sci USA 2014;111:480-485.
42. Teune TM, van der Burg J, van der Moer J, Voogd J, Ruigrok TJ. Topography of cerebellar nuclear projections to the brain stem in the rat. Prog Brain Res 2000;124:141-172.
43. Deniau JM, Kita H, Kitai ST. Patterns of termination of cerebellar and basal ganglia efferents in the rat thalamus. Strictly segregated and partly overlapping projections. Neurosci Lett 1992;144:202-206.
44. Narayanan NS, Laubach M. Methods for studying functional interactions among neuronal populations. Methods Mol Biol 2009;489:135-165.
45. Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM. The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 1989;53:1-31.
46. Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci 2003;23:8432-8444.
47. Fujisawa S, Buzsáki G. A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 2011;72:153-165.
48. Parker KL, Alberico SL, Miller AD, Narayanan NS. Prefrontal D1 dopamine signaling is necessary for temporal expectation during reaction time performance. Neuroscience 2013;255:246-254.
49. Joyal CC, Strazielle C, Lalonde R. Effects of dentate nucleus lesions on spatial and postural sensorimotor learning in rats. Behav Brain Res 2001;122:131-137.
50. Spencer RMC, Ivry RB. Comparison of patients with Parkinson's disease or cerebellar lesions in the production of periodic movements involving eventbased or emergent timing. Brain Cogn 2005;58:84-93.
51. Schutter DJLG, van Honk J, d'Alfonso AAL, Peper JS, Panksepp J. High frequency repetitive transcranial magnetic over the medial cerebellum induces a shift in the prefrontal electroencephalography gamma spectrum: a pilot study in humans. Neurosci Lett 2003;336:73-76.
52. Chen K-H, Okerstrom KL, Kingyon JR, Anderson SW, Cavanagh JF, Narayanan NS. Startle habituation and midfrontal theta activity in Parkinson's disease. J Cogn Neurosci 2016;28:1923-1932.
53. Cavanagh JF. Cortical delta activity reflects reward prediction error and related behavioral adjustments, but at different times. Neuroimage 2015;110:205-216.
54. Laubach M, Caetano MS, Narayanan NS. Mistakes were made: neural mechanisms for the adaptive control of action initiation by the medial prefrontal cortex. J Physiol-Paris 2015;109:104-117.