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01-04-2017 | Original Paper

Electrical Stimulation Normalizes c-Fos Expression in the Deep Cerebellar Nuclei of Depressive-like Rats: Implication of Antidepressant Activity

Authors: Gemma Huguet, Elisabet Kadar, Yasin Temel, Lee Wei Lim

Published in: The Cerebellum | Issue 2/2017

Abstract

The electrical stimulation of specific brain targets has been shown to induce striking antidepressant effects. Despite that recent data have indicated that cerebellum is involved in emotional regulation, the mechanisms by which stimulation improved mood-related behaviors in the cerebellum remained largely obscure. Here, we investigated the stimulation effects of the ventromedial prefrontal cortex (vmPFC), nucleus accumbens (NAc), and lateral habenular nucleus on the c-Fos neuronal activity in various deep cerebellar and vestibular nuclei using the unpredictable chronic mild stress (CMS) animal model of depression. Our results showed that stressed animals had increased number of c-Fos cells in the cerebellar dentate and fastigial nuclei, as well as in the spinal vestibular nucleus. To examine the stimulation effects, we found that vmPFC stimulation significantly decreased the c-Fos activity within the cerebellar fastigial nucleus as compared to the CMS sham. Similarly, there was also a reduction of c-Fos expression in the magnocellular part of the medial vestibular nucleus in vmPFC- and NAc core-stimulated animals when compared to the CMS sham. Correlational analyses showed that the anxiety measure of home-cage emergence escape latency was positively correlated with the c-Fos neuronal activity of the cerebellar fastigial and magnocellular and parvicellular parts of the interposed nuclei in CMS vmPFC-stimulated animals. Interestingly, there was a strong correlation among activation in these cerebellar nuclei, indicating that the antidepressant-like behaviors were possibly mediated by the vmPFC stimulation-induced remodeling within the forebrain-cerebellar neurocircuitry.

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Temel Y, Hescham SA, Jahanshahi A, Janssen ML, Tan SK, van Overbeeke JJ, et al. Neuromodulation in psychiatric disorders. Int Rev Neurobiol. 2012;107:283–314. doi:10.1016/B978-0-12-404706-8.00015-2.CrossRefPubMed

Temel Y, Lim LW. Neurosurgical treatments of depression. Curr Top Behav Neurosci. 2013;14:327–39. doi:10.1007/7854_2012_222.CrossRefPubMed

Lim LW, Tan SK, Groenewegen HJ, Temel Y. Electrical brain stimulation in depression: which target(s)? Biol Psychiatry. 2011, 69:e5-6; author reply e7-8. doi 10.1016/j.biopsych.2010.09.056.

Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, et al. Deep brain stimulation for treatment-resistant depression. Neuron. 2005;45:651–60. doi:10.1016/j.neuron.2005.02.014.CrossRefPubMed

Lim LW, Prickaerts J, Huguet G, Kadar E, Hartung H, Sharp T, et al. Electrical stimulation alleviates depressive-like behaviors of rats: investigation of brain targets and potential mechanisms. Transl Psychiatry. 2015;5:e535. doi:10.1038/tp.2015.24.CrossRefPubMedPubMedCentral

Liu A, Jain N, Vyas A, Lim LW. Ventromedial prefrontal cortex stimulation enhances memory and hippocampal neurogenesis in the middle-aged rats. Elife. 2015, 4. doi 10.7554/eLife.04803.

Lim LW, Janssen ML, Kocabicak E, Temel Y. The antidepressant effects of ventromedial prefrontal cortex stimulation is associated with neural activation in the medial part of the subthalamic nucleus. Behav Brain Res. 2015;279:17–21. doi:10.1016/j.bbr.2014.11.008.CrossRefPubMed

Schlaepfer TE, Bewernick BH, Kayser S, Hurlemann R, Coenen VA. Deep brain stimulation of the human reward system for major depression--rationale, outcomes and outlook. Neuropsychopharmacology. 2014;39:1303–14. doi:10.1038/npp.2014.28.CrossRefPubMedPubMedCentral

Holtzheimer 3rd PE, Mayberg HS. Deep brain stimulation for treatment-resistant depression. Am J Psychiatry. 2010;167:1437–44. doi:10.1176/appi.ajp.2010.10010141.CrossRefPubMedPubMedCentral

10.

Lozano AM, Mayberg HS, Giacobbe P, Hamani C, Craddock RC, Kennedy SH. Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol Psychiatry. 2008;64:461–7. doi:10.1016/j.biopsych.2008.05.034.CrossRefPubMed

11.

Holtzheimer PE, Kelley ME, Gross RE, Filkowski MM, Garlow SJ, Barrocas A, et al. Subcallosal cingulate deep brain stimulation for treatment-resistant unipolar and bipolar depression. Arch Gen Psychiatry. 2012;69:150–8. doi:10.1001/archgenpsychiatry.2011.1456.CrossRefPubMedPubMedCentral

12.

Jimenez F, Velasco F, Salin-Pascual R, Hernandez JA, Velasco M, Criales JL, Nicolini H. A patient with a resistant major depression disorder treated with deep brain stimulation in the inferior thalamic peduncle. Neurosurgery. 2005, 57:585-93; discussion -93.

13.

Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, Axmacher N, et al. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology. 2008;33:368–77. doi:10.1038/sj.npp.1301408.CrossRefPubMed

14.

Bewernick BH, Hurlemann R, Matusch A, Kayser S, Grubert C, Hadrysiewicz B, et al. Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol Psychiatry. 2010;67:110–6. doi:10.1016/j.biopsych.2009.09.013.CrossRefPubMed

15.

Bewernick BH, Kayser S, Sturm V, Schlaepfer TE. Long-term effects of nucleus accumbens deep brain stimulation in treatment-resistant depression: evidence for sustained efficacy. Neuropsychopharmacology. 2012;37:1975–85. doi:10.1038/npp.2012.44.CrossRefPubMedPubMedCentral

16.

Malone Jr DA, Dougherty DD, Rezai AR, Carpenter LL, Friehs GM, Eskandar EN, et al. Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol Psychiatry. 2009;65:267–75. doi:10.1016/j.biopsych.2008.08.029.CrossRefPubMed

17.

Dougherty DD, Rezai AR, Carpenter LL, Howland RH, Bhati MT, O’Reardon JP, et al. A randomized sham-controlled trial of deep brain stimulation of the ventral capsule/ventral striatum for chronic treatment-resistant depression. Biol Psychiatry. 2015;78:240–8. doi:10.1016/j.biopsych.2014.11.023.CrossRefPubMed

18.

Sartorius A, Kiening KL, Kirsch P, von Gall CC, Haberkorn U, Unterberg AW, et al. Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psychiatry. 2010;67:e9–e11. doi:10.1016/j.biopsych.2009.08.027.CrossRefPubMed

19.

Schlaepfer TE, Bewernick BH, Kayser S, Madler B, Coenen VA. Rapid effects of deep brain stimulation for treatment-resistant major depression. Biol Psychiatry. 2013;73:1204–12. doi:10.1016/j.biopsych.2013.01.034.CrossRefPubMed

20.

Temel Y, Tan S, Vlamings R, Sesia T, Lim LW, Lardeux S, Visser-Vandewalle V, Baunez C. Cognitive and limbic effects of deep brain stimulation in preclinical studies. Front Biosci 2009;14(5):1891–1901. doi: 10.2741/3349

21.

Schmahmann JD, Caplan D. Cognition, emotion and the cerebellum. Brain. 2006;129:290–2. doi:10.1093/brain/awh729.CrossRefPubMed

22.

Schmahmann JD. From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Hum Brain Mapp. 1996, 4:174-98. doi 10.1002/(SICI)1097-0193(1996)4:3<174::AID-HBM3>3.0.CO;2-0 10.1002/(SICI)1097-0193(1996)4:3<174::AID-HBM3>3.0.CO;2-0.

23.

Moers-Hornikx VM, Sesia T, Basar K, Lim LW, Hoogland G, Steinbusch HW, et al. Cerebellar nuclei are involved in impulsive behaviour. Behav Brain Res. 2009;203:256–63. doi:10.1016/j.bbr.2009.05.011.CrossRefPubMed

24.

Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010;46:831–44. doi:10.1016/j.cortex.2009.11.008.CrossRefPubMedPubMedCentral

25.

Moers-Hornikx VM, Vles JS, Lim LW, Ayyildiz M, Kaplan S, Gavilanes AW, et al. Periaqueductal grey stimulation induced panic-like behaviour is accompanied by deactivation of the deep cerebellar nuclei. Cerebellum. 2011;10:61–9. doi:10.1007/s12311-010-0228-z.CrossRefPubMed

26.

Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4):561–79.CrossRefPubMed

27.

Grieve SM, Korgaonkar MS, Koslow SH, Gordon E, Williams LM. Widespread reductions in gray matter volume in depression. Neuroimage Clin. 2013;3:332–9. doi:10.1016/j.nicl.2013.08.016.CrossRefPubMedPubMedCentral

28.

Liang MJ, Zhou Q, Yang KR, Yang XL, Fang J, Chen WL, et al. Identify changes of brain regional homogeneity in bipolar disorder and unipolar depression using resting-state FMRI. PLoS One. 2013;8:e79999. doi:10.1371/journal.pone.0079999.CrossRefPubMedPubMedCentral

29.

Guo W, Liu F, Liu J, Yu L, Zhang Z, Zhang J, et al. Is there a cerebellar compensatory effort in first-episode, treatment-naive major depressive disorder at rest? Prog Neuropsychopharmacol Biol Psychiatry. 2013;46:13–8. doi:10.1016/j.pnpbp.2013.06.009.CrossRefPubMed

30.

Jiang WH, Yuan YG, Zhou H, Bai F, You JY, Zhang ZJ. Abnormally altered patterns of whole brain functional connectivity network of posterior cingulate cortex in remitted geriatric depression: a longitudinal study. CNS Neurosci Ther. 2014;20:772–7. doi:10.1111/cns.12250.CrossRefPubMed

31.

Frank B, Andrzejewski K, Goricke S, Wondzinski E, Siebler M, Wild B, et al. Humor, laughter, and the cerebellum: insights from patients with acute cerebellar stroke. Cerebellum. 2013;12:802–11. doi:10.1007/s12311-013-0488-5.CrossRefPubMed

32.

Akil H, Statham PF, Gotz M, Bramley P, Whittle IR. Adult cerebellar mutism and cognitive-affective syndrome caused by cystic hemangioblastoma. Acta Neurochir (Wien). 2006;148:597–8. doi:10.1007/s00701-005-0646-8.CrossRef

33.

Diaconescu AO, Kramer E, Hermann C, Ma Y, Dhawan V, Chaly T, et al. Distinct functional networks associated with improvement of affective symptoms and cognitive function during citalopram treatment in geriatric depression. Hum Brain Mapp. 2011;32:1677–91. doi:10.1002/hbm.21135.CrossRefPubMed

34.

Zeng LL, Liu L, Liu Y, Shen H, Li Y, Hu D. Antidepressant treatment normalizes white matter volume in patients with major depression. PLoS One. 2012;7:e44248. doi:10.1371/journal.pone.0044248.CrossRefPubMedPubMedCentral

35.

Chiu R, Boyle WJ, Meek J, Smeal T, Hunter T, Karin M. The c-Fos protein interacts with c-Jun/AP-1 to stimulate transcription of AP-1 responsive genes. Cell. 1988;54:541–52.CrossRefPubMed

36.

Hestermann D, Temel Y, Blokland A, Lim LW. Acute serotonergic treatment changes the relation between anxiety and HPA-axis functioning and periaqueductal gray activation. Behav Brain Res 2014, 273:155-65. doi 10.1016/j.bbr.2014.07.003.

37.

Lim LW, Blokland A, van Duinen M, Visser-Vandewalle V, Tan S, Vlamings R, Janssen M, Jahanshahi A, Aziz-Mohammadi M, Steinbusch HW, Schruers K, Temel Y. Increased plasma corticosterone levels after periaqueductal gray stimulation-induced escape reaction or panic attacks in rats. Behav Brain Res 2011, 218:301-7. doi 10.1016/j.bbr.2010.12.026.

38.

Lim LW, Temel Y, Visser-Vandewalle V, Blokland A, Steinbusch H. Fos immunoreactivity in the rat forebrain induced by electrical stimulation of the dorsolateral periaqueductal gray matter. J Chem Neuroanat. 2009;38:83–96. doi:10.1016/j.jchemneu.2009.06.011.CrossRefPubMed

39.

Temel Y, Blokland A, Lim LW. Deactivation of the parvalbumin-positive interneurons in the hippocampus after fear-like behaviour following electrical stimulation of the dorsolateral periaqueductal gray of rats. Behav Brain Res. 2012;233:322–5. doi:10.1016/j.bbr.2012.05.029.CrossRefPubMed

40.

Lim LW, Temel Y, Sesia T, Vlamings R, Visser-Vandewalle V, Steinbusch HW and Blokland A. Buspirone induced acute and chronic changes of neural activation in the periaqueductal gray of rats. Neuroscience. 2008, 155:164-73. doi 10.1016/j.neuroscience.2008.05.038.

41.

Lim LW, Blokland A, Tan S, Vlamings R, Sesia T, Aziz-Mohammadi M, Visser-Vandewalle V, Steinbusch HW, Schruers K, Temel Y. Attenuation of fear-like response by escitalopram treatment after electrical stimulation of the midbrain dorsolateral periaqueductal gray. Exp Neurol. 2010, 226:293-300. doi 10.1016/j.expneurol.2010.08.035.

42.

Tan S, Vlamings R, Lim L, Sesia T, Janssen ML, Steinbusch HW, Visser-Vandewalle V, Temel Y. Experimental deep brain stimulation in animal models. Neurosurgery. 2010, 67:1073-9; discussion80. doi 10.1227/NEU.0b013e3181ee3580.

43.

Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. China: Academic Press of Elsevier; 2007.

44.

Moers-Hornikx VMP, Vles JSH, Hemmes RJM, Lim LW, Hoogland G, Steinbusch HWM, et al. c-Fos expression in the deep cerebellar nuclei in a rat model of conditioned fear. J Exp Clin Med. 2012;29:201–7. doi:10.5835/jecm.omu.29.03.007.CrossRef

45.

Sullivan RM, Dufresne MM, Waldron J. Lateralized sex differences in stress-induced dopamine release in the rat. Neuroreport. 2009;20:229–32. doi:10.1097/WNR.0b013e3283196b3e.CrossRefPubMed

46.

Weathington JM, Puhy C, Hamki A, Strahan JA, Cooke BM. Sexually dimorphic patterns of neural activity in response to juvenile social subjugation. Behav Brain Res. 2013;256:464–71. doi:10.1016/j.bbr.2013.08.042.CrossRefPubMed

47.

Schulz KM, Andrud KM, Burke MB, Pearson JN, Kreisler AD, Stevens KE, et al. The effects of prenatal stress on alpha4 beta2 and alpha7 hippocampal nicotinic acetylcholine receptor levels in adult offspring. Dev Neurobiol. 2013;73:806–14. doi:10.1002/dneu.22097.PubMedPubMedCentral

48.

Soza Ried AM, Aviles M. Asymmetries of vestibular dysfunction in major depression. Neuroscience. 2007;144:128–34. doi:10.1016/j.neuroscience.2006.09.023.CrossRefPubMed

49.

Kilts CD, Kelsey JE, Knight B, Ely TD, Bowman FD, Gross RE, et al. The neural correlates of social anxiety disorder and response to pharmacotherapy. Neuropsychopharmacology. 2006;31:2243–53. doi:10.1038/sj.npp.1301053.CrossRefPubMed

50.

Warwick JM, Carey P, Jordaan GP, Dupont P, Stein DJ. Resting brain perfusion in social anxiety disorder: a voxel-wise whole brain comparison with healthy control subjects. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:1251–6. doi:10.1016/j.pnpbp.2008.03.017.CrossRefPubMed

51.

Bremner JD, Narayan M, Staib LH, Southwick SM, McGlashan T, Charney DS. Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. Am J Psychiatry. 1999;156:1787–95. doi:10.1176/ajp.156.11.1787.PubMedPubMedCentral

52.

Bonne O, Gilboa A, Louzoun Y, Brandes D, Yona I, Lester H, et al. Resting regional cerebral perfusion in recent posttraumatic stress disorder. Biol Psychiatry. 2003;54:1077–86.CrossRefPubMed

53.

Blair K, Shaywitz J, Smith BW, Rhodes R, Geraci M, Jones M, et al. Response to emotional expressions in generalized social phobia and generalized anxiety disorder: evidence for separate disorders. Am J Psychiatry. 2008;165:1193–202. doi:10.1176/appi.ajp.2008.07071060.CrossRefPubMedPubMedCentral

54.

Allen G, McColl R, Barnard H, Ringe WK, Fleckenstein J, Cullum CM. Magnetic resonance imaging of cerebellar-prefrontal and cerebellar-parietal functional connectivity. Neuroimage. 2005;28:39–48. doi:10.1016/j.neuroimage.2005.06.013.CrossRefPubMed

55.

Kamali A, Kramer LA, Frye RE, Butler IJ, Hasan KM. Diffusion tensor tractography of the human brain cortico-ponto-cerebellar pathways: a quantitative preliminary study. J Magn Reson Imaging. 2010;32:809–17. doi:10.1002/jmri.22330.CrossRefPubMedPubMedCentral

56.

Leergaard TB, Bjaalie JG. Topography of the complete corticopontine projection: from experiments to principal Maps. Front Neurosci. 2007;1:211–23. doi:10.3389/neuro.01.1.1.016.2007.CrossRefPubMedPubMedCentral

57.

Rogers TD, Dickson PE, Heck DH, Goldowitz D, Mittleman G, Blaha CD. Connecting the dots of the cerebro-cerebellar role in cognitive function: neuronal pathways for cerebellar modulation of dopamine release in the prefrontal cortex. Synapse. 2011;65:1204–12. doi:10.1002/syn.20960.CrossRefPubMed

58.

Lalonde R, Strazielle C. The effects of cerebellar damage on maze learning in animals. Cerebellum. 2003;2:300–9. doi:10.1080/14734220310017456.CrossRefPubMed

59.

Dum RP, Li C, Strick PL. Motor and nonmotor domains in the monkey dentate. Ann N Y Acad Sci. 2002;978:289–301.CrossRefPubMed

60.

Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89:634–9. doi:10.1152/jn.00626.2002.CrossRefPubMed

61.

Schmahmann JD. The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol Rev. 1982;2010(20):236–60. doi:10.1007/s11065-010-9142-x.

62.

Nashold Jr BS, Slaughter DG. Effects of stimulating or destroying the deep cerebellar regions in man. J Neurosurg. 1969;31:172–86. doi:10.3171/jns.1969.31.2.0172.CrossRefPubMed

63.

Bauer DJ, Kerr AL, Swain RA. Cerebellar dentate nuclei lesions reduce motivation in appetitive operant conditioning and open field exploration. Neurobiol Learn Mem. 2011;95:166–75. doi:10.1016/j.nlm.2010.12.009.CrossRefPubMed

64.

Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6:254–67. doi:10.1080/14734220701490995.CrossRefPubMed

65.

Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, et al. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain. 2007;130:630–53. doi:10.1093/brain/awl359.CrossRefPubMed

66.

Rapkin AJ, Berman SM, Mandelkern MA, Silverman DH, Morgan M, London ED. Neuroimaging evidence of cerebellar involvement in premenstrual dysphoric disorder. Biol Psychiatry. 2011;69:374–80. doi:10.1016/j.biopsych.2010.09.029.CrossRefPubMed

67.

Rijkers K, Moers-Hornikx VM, Hemmes RJ, Aalbers MW, Temel Y, Vles JS, et al. Sustained reduction of cerebellar activity in experimental epilepsy. Biomed Res Int. 2015;2015:718591. doi:10.1155/2015/718591.CrossRefPubMedPubMedCentral

68.

Nakayama K, Kiyosue K, Taguchi T. Diminished neuronal activity increases neuron-neuron connectivity underlying silent synapse formation and the rapid conversion of silent to functional synapses. J Neurosci. 2005;25:4040–51. doi:10.1523/JNEUROSCI.4115-04.2005.CrossRefPubMed

69.

Burrone J, O’Byrne M, Murthy VN. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature. 2002;420:414–8. doi:10.1038/nature01242.CrossRefPubMed

70.

Lu X, Miyachi S, Takada M. Anatomical evidence for the involvement of medial cerebellar output from the interpositus nuclei in cognitive functions. Proc Natl Acad Sci U S A. 2012;109:18980–4. doi:10.1073/pnas.1211168109.CrossRefPubMedPubMedCentral

71.

Wu GY, Yao J, Fan ZL, Zhang LQ, Li X, Zhao CD, et al. Classical eyeblink conditioning using electrical stimulation of caudal mPFC as conditioned stimulus is dependent on cerebellar interpositus nucleus in guinea pigs. Acta Pharmacol Sin. 2012;33:717–27. doi:10.1038/aps.2012.32.CrossRefPubMedPubMedCentral

72.

Wang YJ, Chen H, Hu C, Ke XF, Yang L, Xiong Y, et al. Baseline theta activities in medial prefrontal cortex and deep cerebellar nuclei are associated with the extinction of trace conditioned eyeblink responses in guinea pigs. Behav Brain Res. 2014;275:72–83. doi:10.1016/j.bbr.2014.08.059.CrossRefPubMed

73.

Carleton SC, Carpenter MB. Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res. 1983;278:29–51.CrossRefPubMed

74.

Godemann F, Linden M, Neu P, Heipp E, Dorr P. A prospective study on the course of anxiety after vestibular neuronitis. J Psychosom Res. 2004;56:351–4. doi:10.1016/S0022-3999(03)00079-5.CrossRefPubMed

75.

Godemann F, Siefert K, Hantschke-Bruggemann M, Neu P, Seidl R, Strohle A. What accounts for vertigo one year after neuritis vestibularis—anxiety or a dysfunctional vestibular organ? J Psychiatr Res. 2005;39:529–34. doi:10.1016/j.jpsychires.2004.12.006.CrossRefPubMed

76.

Kalueff AV, Ishikawa K, Griffith AJ. Anxiety and otovestibular disorders: linking behavioral phenotypes in men and mice. Behav Brain Res. 2008;186:1–11. doi:10.1016/j.bbr.2007.07.032.CrossRefPubMed

77.

Smith PF, Zheng Y, Horii A, Darlington CL. Does vestibular damage cause cognitive dysfunction in humans? J Vestib Res. 2005;15:1–9.PubMed

78.

Halberstadt AL, Balaban CD. Organization of projections from the raphe nuclei to the vestibular nuclei in rats. Neuroscience. 2003;120:573–94.CrossRefPubMed

79.

Balaban CD. Neural substrates linking balance control and anxiety. Physiol Behav. 2002;77:469–75.CrossRefPubMed

80.

Gray JA, McNaughton N. The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septohippocampal System, 2nd Edition..Oxford University Press 2000.

81.

Halberstadt AL, Balaban CD. Anterograde tracing of projections from the dorsal raphe nucleus to the vestibular nuclei. Neuroscience. 2006;143:641–54. doi:10.1016/j.neuroscience.2006.08.013.CrossRefPubMed

82.

Halberstadt AL, Balaban CD. Serotonergic and nonserotonergic neurons in the dorsal raphe nucleus send collateralized projections to both the vestibular nuclei and the central amygdaloid nucleus. Neuroscience. 2006;140:1067–77. doi:10.1016/j.neuroscience.2006.02.053.CrossRefPubMed

83.

Wulff P, Schonewille M, Renzi M, Viltono L, Sassoe-Pognetto M, Badura A, et al. Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci. 2009;12:1042–9. doi:10.1038/nn.2348.CrossRefPubMedPubMedCentral

84.

Verduzco-Flores S. Stochastic synchronization in purkinje cells with feedforward inhibition could be studied with equivalent phase-response curves. J Math Neurosci. 2015;5:25. doi:10.1186/s13408-015-0025-6.CrossRefPubMed

85.

Chen H, Wang YJ, Yang L, Sui JF, Hu ZA, Hu B. Theta synchronization between medial prefrontal cortex and cerebellum is associated with adaptive performance of associative learning behavior. Sci Rep. 2016;6:20960. doi:10.1038/srep20960.CrossRefPubMedPubMedCentral

Title: Electrical Stimulation Normalizes c-Fos Expression in the Deep Cerebellar Nuclei of Depressive-like Rats: Implication of Antidepressant Activity
Authors: Gemma Huguet
Elisabet Kadar
Yasin Temel
Lee Wei Lim
Publication date: 01-04-2017
Publisher: Springer US
Published in: The Cerebellum / Issue 2/2017
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI: https://doi.org/10.1007/s12311-016-0812-y

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Electrical Stimulation Normalizes c-Fos Expression in the Deep Cerebellar Nuclei of Depressive-like Rats: Implication of Antidepressant Activity

Abstract

Keynote webinar | Spotlight on medication adherence

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Abstract

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