Chronic deep brain stimulation of the rat ventral medial prefrontal cortex disrupts hippocampal-prefrontal coherence

Experimental Neurology

Volumn 269, Issue , 2015, Pages 1-7

  Insel, Nathan ^a   Pilkiw, Maryna ^b   Nobrega, José N ^a,b   Hutchison, William D ^c   Takehara Nishiuchi, Kaori ^b   Hamani, Clement ^a,c  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

Delta; Depression; Functional connectivity; Oscillations; Synchrony

Indexed keywords

FLUOXETINE; SEROTONIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; AUDITORY STIMULATION; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; COHERENCE; CONTROLLED STUDY; DEPRESSION; ELECTRODE IMPLANT; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EVENT RELATED POTENTIAL; EVOKED AUDITORY RESPONSE; HIPPOCAMPUS; LIMBIC CORTEX; LONG TERM CARE; MALE; NERVE CELL NETWORK; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; THETA RHYTHM; TREATMENT OUTCOME; VENTROMEDIAL PREFRONTAL CORTEX; ANIMAL; CINGULATE GYRUS; DEPRESSIVE DISORDER; DISEASE MODEL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT;

ANIMALS; DEEP BRAIN STIMULATION; DEPRESSION; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; GYRUS CINGULI; HIPPOCAMPUS; MALE; NERVE NET; PREFRONTAL CORTEX; RATS, SPRAGUE-DAWLEY;

EID: 84926471726     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.03.023     Document Type: Article

References (46)

1. Adhikari A., Topiwala M.A., Gordon J.A. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 2010, 65:257-269. 10.1016/j.neuron.2009.12.002.
2. Bayer H.M., Lau B., Glimcher P.W. Statistics of midbrain dopamine neuron spike trains in the awake primate. J. Neurophysiol. 2007, 98:1428-1439. 10.1152/jn.01140.2006.
3. Benchenane K., Peyrache A., Khamassi M., Tierney P.L., Gioanni Y., Battaglia F.P., Wiener S.I. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 2010, 66:921-936. 10.1016/j.neuron.2010.05.013.
4. Berman M.G., Peltier S., Nee D.E., Kross E., Deldin P.J., Jonides J. Depression, rumination and the default network. Soc. Cogn. Affect. Neurosci. 2011, 6:548-555. 10.1093/scan/nsq080.
5. Beyer C.E., Cremers T.I.F.H. Do selective serotonin reuptake inhibitors acutely increase frontal cortex levels of serotonin?. Eur. J. Pharmacol. 2008, 580:350-354. 10.1016/j.ejphar.2007.11.028.
6. Broadway J.M., Holtzheimer P.E., Hilimire M.R., Parks N.A., Devylder J.E., Mayberg H.S., Corballis P.M. Frontal theta cordance predicts 6-month antidepressant response to subcallosal cingulate deep brain stimulation for treatment-resistant depression: a pilot study. Neuropsychopharmacology 2012, 37:1764-1772. 10.1038/npp.2012.23.
7. Colgin L.L. Oscillations and hippocampal-prefrontal synchrony. Curr. Opin. Neurobiol. 2011, 21:467-474. 10.1016/j.conb.2011.04.006.
8. Davey C.G., Yücel M., Allen N.B., Harrison B.J. Task-related deactivation and functional connectivity of the subgenual cingulate cortex in major depressive disorder. Front. Psychiatry 2012, 3:14. 10.3389/fpsyt.2012.00014.
9. Drevets W.C., Bogers W., Raichle M.E. Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism. Eur. Neuropsychopharmacol. 2002, 12:527-544.
10. Dzirasa K., Coque L., Sidor M.M., Kumar S., Dancy E.A., Takahashi J.S., McClung C.A., Nicolelis M.A.L. Lithium ameliorates nucleus accumbens phase-signaling dysfunction in a genetic mouse model of mania. J. Neurosci. 2010, 30:16314-16323. 10.1523/JNEUROSCI. 4289-10.2010.
11. Fingelkurts A.A., Fingelkurts A.A., Rytsälä H., Suominen K., Isometsä E., Kähkönen S. Impaired functional connectivity at EEG alpha and theta frequency bands in major depression. Hum. Brain Mapp. 2007, 28:247-261. 10.1002/hbm.20275.
12. Fujisawa S., Buzsáki G. A 4Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 2011, 72:153-165. 10.1016/j.neuron.2011.08.018.
13. Greicius M.D., Flores B.H., Menon V., Glover G.H., Solvason H.B., Kenna H., Reiss A.L., Schatzberg A.F. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 2007, 62:429-437. 10.1016/j.biopsych.2006.09.020.
14. Hamani C., Diwan M., Macedo C.E., Brandão M.L., Shumake J., Gonzalez-Lima F., Raymond R., Lozano A.M., Fletcher P.J., Nobrega J.N. Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats. Biol. Psychiatry 2010, 67:117-124. 10.1016/j.biopsych.2009.08.025.
15. Hamani C., Machado D.C., Hipólide D.C., Dubiela F.P., Suchecki D., Macedo C.E., Tescarollo F., Martins U., Covolan L., Nobrega J.N. Deep brain stimulation reverses anhedonic-like behavior in a chronic model of depression: role of serotonin and brain derived neurotrophic factor. Biol. Psychiatry 2012, 71:30-35. 10.1016/j.biopsych.2011.08.025.
16. Hamani C., Amorim B.O., Wheeler A.L., Diwan M., Driesslein K., Covolan L., Butson C.R., Nobrega J.N. Deep brain stimulation in rats: different targets induce similar antidepressant-like effects but influence different circuits. Neurobiol. Dis. 2014, 71:205-214. 10.1016/j.nbd.2014.08.007.
17. Hartwich K., Pollak T., Klausberger T. Distinct firing patterns of identified basket and dendrite-targeting interneurons in the prefrontal cortex during hippocampal theta and local spindle oscillations. J. Neurosci. 2009, 29:9563-9574. 10.1523/JNEUROSCI. 1397-09.2009.
18. Hoover W.B., Vertes R.P. Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct. Funct. 2007, 212:149-179. 10.1007/s00429-007-0150-4.
19. Hyland B.I., Reynolds J.N.J., Hay J., Perk C.G., Miller R. Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 2002, 114:475-492.
20. Hyman J.M., Zilli E.A., Paley A.M., Hasselmo M.E. Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus 2005, 15:739-749. 10.1002/hipo.20106.
21. Hyman J.M., Zilli E.A., Paley A.M., Hasselmo M.E. Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates. Front. Integr. Neurosci. 2010, 4:2. 10.3389/neuro.07.002.2010.
22. Jay T.M., Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 1991, 313:574-586. 10.1002/cne.903130404.
23. Jay T.M., Glowinski J., Thierry A.M. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res. 1989, 505:337-340.
24. Jones M.W., Wilson M.A. Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 2005, 15:867-873. 10.1002/hipo.20119.
25. Jones M.W., Wilson M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 2005, 3:e402. 10.1371/journal.pbio.0030402.
26. Jones B.F., Witter M.P. Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus 2007, 17:957-976. 10.1002/hipo.20330.
27. Kennedy S.H., Evans K.R., Krüger S., Mayberg H.S., Meyer J.H., McCann S., Arifuzzman A.I., Houle S., Vaccarino F.J. Changes in regional brain glucose metabolism measured with positron emission tomography after paroxetine treatment of major depression. Am. J. Psychiatry 2001, 158:899-905.
28. Kobayashi S., Schultz W. Influence of reward delays on responses of dopamine neurons. J. Neurosci. 2008, 28:7837-7846. 10.1523/JNEUROSCI. 1600-08.2008.
29. Kramis R., Vanderwolf C.H., Bland B.H. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol. 1975, 49:58-85.
30. Laroche S., Davis S., Jay T.M. Plasticity at hippocampal to prefrontal cortex synapses: dual roles in working memory and consolidation. Hippocampus 2000, 10:438-446. 10.1002/1098-1063(2000)10:4<438::AID-HIPO10>3.0.CO;2-3.
31. Leuchter A.F., Cook I.A., Hunter A.M., Cai C., Horvath S. Resting-state quantitative electroencephalography reveals increased neurophysiologic connectivity in depression. PLoS One 2012, 7:e32508. 10.1371/journal.pone.0032508.
32. Lozano A.M., Mayberg H.S., Giacobbe P., Hamani C., Craddock R.C., Kennedy S.H. Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol. Psychiatry 2008, 64:461-467. 10.1016/j.biopsych.2008.05.034.
33. Mayberg H.S., Liotti M., Brannan S.K., McGinnis S., Mahurin R.K., Jerabek P.A., Silva J.A., Tekell J.L., Martin C.C., Lancaster J.L., Fox P.T. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am. J. Psychiatry 1999, 156:675-682. 10.1176/ajp.156.5.675.
34. Mayberg H.S., Lozano A.M., Voon V., McNeely H.E., Seminowicz D., Hamani C., Schwalb J.M., Kennedy S.H. Deep brain stimulation for treatment-resistant depression. Neuron 2005, 45:651-660. 10.1016/j.neuron.2005.02.014.
35. Paladini C.A., Tepper J.M. GABA(A) and GABA(B) antagonists differentially affect the firing pattern of substantia nigra dopaminergic neurons in vivo. Synapse 1999, 32:165-176. 10.1002/(SICI)1098-2396(19990601)32:3<165::AID-SYN3>3.0.CO;2-N.
36. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego. 4th ed.
37. Quraan M.A., Protzner A.B., Daskalakis Z.J., Giacobbe P., Tang C.W., Kennedy S.H., Lozano A.M., McAndrews M.P. EEG power asymmetry and functional connectivity as a marker of treatment effectiveness in DBS surgery for depression. Neuropsychopharmacology 2014, 39:1270-1281. 10.1038/npp.2013.330.
38. Sabol K.E., Richards J.B., Seiden L.S. Fluoxetine attenuates the DL-fenfluramine-induced increase in extracellular serotonin as measured by in vivo dialysis. Brain Res. 1992, 585:421-424.
39. Sambataro F., Wolf N.D., Pennuto M., Vasic N., Wolf R.C. Revisiting default mode network function in major depression: evidence for disrupted subsystem connectivity. Psychol. Med. 2013, 1-11. 10.1017/S0033291713002596.
40. Siapas A.G., Lubenov E.V., Wilson M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 2005, 46:141-151. 10.1016/j.neuron.2005.02.028.
41. Sirota A., Montgomery S., Fujisawa S., Isomura Y., Zugaro M., Buzsáki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 2008, 60:683-697. 10.1016/j.neuron.2008.09.014.
42. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
43. Swanson L.W. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res. 1981, 217:150-154.
44. Wheeler A.L., Teixeira C.M., Wang A.H., Xiong X., Kovacevic N., Lerch J.P., McIntosh A.R., Parkinson J., Frankland P.W. Identification of a functional connectome for long-term fear memory in mice. PLoS Comput. Biol. 2013, 9:e1002853. 10.1371/journal.pcbi.1002853.
45. Young C.K., McNaughton N. Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cereb. Cortex 2009, 19:24-40. 10.1093/cercor/bhn055.
46. Zeng L.-L., Shen H., Liu L., Wang L., Li B., Fang P., Zhou Z., Li Y., Hu D. Identifying major depression using whole-brain functional connectivity: a multivariate pattern analysis. Brain 2012, 135:1498-1507. 10.1093/brain/aws059.