Optogenetic activation of CA1 pyramidal neurons at the dorsal and ventral hippocampus evokes distinct brain-wide responses revealed by mouse fMRI

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Takata, Norio ^a,b   Yoshida, Keitaro ^a   Komaki, Yuji ^a,b   Xu, Ming ^a   Sakai, Yuki ^a,b,c   Hikishima, Keigo ^a,b   Mimura, Masaru ^a   Okano, Hideyuki ^a   Tanaka, Kenji F ^a  

^a KEIO UNIVERSITY   (Japan)

^b CENTRAL INSTITUTE FOR EXPERIMENTAL ANIMALS   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNEL RHODOPSIN 2; RHODOPSIN; UNCLASSIFIED DRUG; CHANNELRHODOPSIN 2, MOUSE; GLASS FIBER; OXYGEN;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOLD SIGNAL; BRAIN REGION; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; ELECTROPHYSIOLOGY; EVOKED CORTICAL RESPONSE; FEMALE; FREQUENCY MODULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAMMA RHYTHM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IN VIVO STUDY; LATERAL SEPTUM; LOCAL FIELD POTENTIAL; MALE; MOUSE; MULTI UNIT ACTIVITY; NONHUMAN; OPTOGENETICS; PYRAMIDAL NERVE CELL; RETROSPLENIAL CORTEX; THETA RHYTHM; TRANSGENIC MOUSE; VENTRAL HIPPOCAMPUS; ACTION POTENTIAL; ANIMAL; BLOOD; ELECTROSTIMULATION; IMPLANT; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES;

MUS MUSCULUS;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; ELECTRIC STIMULATION; IMPLANTS, EXPERIMENTAL; MAGNETIC RESONANCE IMAGING; MICE, TRANSGENIC; OPTICAL FIBERS; OPTOGENETICS; OXYGEN; PYRAMIDAL CELLS; RHODOPSIN;

EID: 84925625642     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121417     Document Type: Article

References (51)

1. Fanselow MS, Dong H-W. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron. 2010; 65: 7-19. doi: 10.1016/j.neuron.2009.11.031 PMID: 20152109
2. Moser E, Moser MB, Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci. 1993; 13: 3916-3925. PMID: 8366351
3. Hughes KR. Dorsal and ventral hippocampus lesions and maze learning: influence of preoperative environment. Can J Psychol. 1965; 19: 325-332. PMID: 5847750
4. Kjelstrup KG, Tuvnes FA, Steffenach H-A, Murison R, Moser EI, Moser M-B. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA. 2002; 99: 10825-10830. doi: 10.1073/pnas.152112399 PMID: 12149439
5. Ferbinteanu J, Ray C, McDonald RJ. Both dorsal and ventral hippocampus contribute to spatial learning in Long - Evans rats. Neuroscience Letters. 2003; 345: 131-135. doi: 10.1016/S0304-3940(03)00473-7 PMID: 12821188
6. Rudy JW, Matus-Amat P. The ventral hippocampus supports a memory representation of context and contextual fear conditioning: implications for a unitary function of the hippocampus. Behav Neurosci. 2005; 119: 154-163. doi: 10.1037/0735-7044.119.1.154 PMID: 15727521
7. Jung MW, Wiener SI, McNaughton BL. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci. 1994; 14: 7347-7356. PMID: 7996180
8. Cenquizca LA, Swanson LW. Analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat. The Journal of Comparative Neurology. 2006; 497: 101-114. doi: 10.1002/cne.20985 PMID: 16680763
9. Cenquizca LA, Swanson LW. Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Research Reviews. 2007; 56: 1-26. doi: 10.1016/j.brainresrev.2007.05.002 PMID: 17559940
10. Lee JH, Durand R, Gradinaru V, Zhang F, Goshen I, Kim D-S, et al. Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature. 2010; 465: 788-792. doi: 10.1038/nature09108 PMID: 20473285
11. Tanaka KF, Matsui K, Sasaki T, Sano H, Sugio S, Fan K, et al. Expanding the repertoire of optogenetically targeted cells with an enhanced gene expression system. Cell Rep. 2012; 2: 397-406. doi: 10.1016/j.celrep.2012.06.011 PMID: 22854021
12. Baltes C, Bosshard S, Mueggler T, Ratering D, Rudin M. Increased blood oxygen level-dependent (BOLD) sensitivity in the mouse somatosensory cortex during electrical forepaw stimulation using a cryogenic radiofrequency probe. NMR Biomed. 2011; 24: 439-446. doi: 10.1002/nbm.1613 PMID: 22945293
13. Adamczak JM, Farr TD, Seehafer JU, Kalthoff D, Hoehn M. High field BOLD response to forepaw stimulation in the mouse. Neuroimage. 2010; 51: 704-712. doi: 10.1016/j.neuroimage.2010.02.083 PMID: 20211267
14. Seki F, Hikishima K, Nambu S, Okanoya K, Okano HJ, Sasaki E, et al. Multidimensional MRI-CT atlas of the naked mole-rat brain (Heterocephalus glaber). Front Neuroanat. 2013; 7: 45. doi: 10.3389/fnana.2013.00045 PMID: 24391551
15. Song X-W, Dong Z-Y, Long X-Y, Li S-F, Zuo X-N, Zhu C-Z, et al. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE. 2011; 6: e25031. doi: 10.1371/journal.pone.0025031 PMID: 21949842
16. Franklin KBJ, Paxinos G. The mouse brain in stereotaxic coordinates. Amsterdam: Boston: Elsevier/Academic Press; 2008.
17. Buzsáki G, Buhl DL, Harris KD, Csicsvari J, Czéh B, Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience. 2003; 116: 201-211. doi: 10.1016/S0306-4522(02)00669-3 PMID: 12535953
18. Quiroga RQ, Nadasdy Z, Ben-Shaul Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 2004; 16: 1661-1687. doi: 10.1162/089976604774201631 PMID: 15228749
19. Stark E, Roux L, Eichler R, Senzai Y, Royer S, Buzsáki G. Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations. Neuron. 2014; 83: 467-480. doi: 10.1016/j.neuron.2014.06.023 PMID: 25033186
20. Morgan JI, Cohen DR, Hempstead JL, Curran T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science. 1987; 237: 192-197. doi: 10.1126/science.3037702 PMID: 3037702
21. Cowansage KK, Shuman T, Dillingham BC, Chang A, Golshani P, Mayford M. Direct Reactivation of a Coherent Neocortical Memory of Context. Neuron. 2014; doi: 10.1016/j.neuron.2014.09.022
22. Jinno S. Structural organization of long-range GABAergic projection system of the hippocampus. Front Neuroanat. 2009; 3: 13. doi: 10.3389/neuro.05.013.2009 PMID: 19649167
23. Buzsáki G, Geisler C, Henze DA, Wang X-J. Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons. Trends Neurosci. 2004; 27: 186-193. doi: 10.1016/j.tins.2004.02.007 PMID: 15046877
24. Chaudhury D, Walsh JJ, Friedman AK, Juarez B, Ku SM, Koo JW, et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature. 2013; 493: 532-536. doi: 10.1038/nature11713 PMID: 23235832
25. Angenstein F, Kammerer E, Niessen HG, Frey JU, Scheich H, Frey S. Frequency-dependent activation pattern in the rat hippocampus, a simultaneous electrophysiological and fMRI study. NeuroImage. 2007; 38: 150-163. doi: 10.1016/j.neuroimage.2007.07.022 PMID: 17728153
26. Canals S, Beyerlein M, Murayama Y, Logothetis NK. Electric stimulation fMRI of the perforant pathway to the rat hippocampus. Magn Reson Imaging. 2008; 26: 978-986. doi: 10.1016/j.mri.2008.02.018 PMID: 18479870
27. Canals S, Beyerlein M, Merkle H, Logothetis NK. Functional MRI Evidence for LTP-Induced Neural Network Reorganization. Current Biology. 2009; 19: 398-403. doi: 10.1016/j.cub.2009.01.037 PMID: 19230667
28. McLennan H, Miller JJ. The hippocampal control of neuronal discharges in the septum of the rat. J Physiol (Lond). 1974; 237: 607-624. PMID: 4596602
29. Mello LEAM, Tan AM, Finch DM. Convergence of projections from the rat hippocampal formation, medial geniculate and basal forebrain onto single amygdaloid neurons: an in vivo extra- and intracellular electrophysiological study. Brain Research. 1992; 587: 24-40. doi: 10.1016/0006-8993(92)91425-E PMID: 1525648
30. Huttunen JK, Gröhn O, Penttonen M. Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. NeuroImage. 2008; 39: 775-785. doi: 10.1016/j.neuroimage.2007.06.042 PMID: 17964186
31. Dougherty KA, Islam T, Johnston D. Intrinsic excitability of CA1 pyramidal neurones from the rat dorsal and ventral hippocampus. J Physiol (Lond). 2012; 590: 5707-5722. doi: 10.1113/jphysiol.2012.242693 PMID: 22988138
32. Patel J, Fujisawa S, Berényi A, Royer S, Buzsáki G. Traveling Theta Waves along the Entire Septotemporal Axis of the Hippocampus. Neuron. 2012; 75: 410-417. doi: 10.1016/j.neuron.2012.07.015 PMID: 22884325
33. Stark E, Koos T, Buzsáki G. Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. Journal of Neurophysiology. 2012; 108: 349-363. doi: 10.1152/jn.00153.2012 PMID: 22496529
34. Abe Y, Sekino M, Terazono Y, Ohsaki H, Fukazawa Y, Sakai S, et al. Opto-fMRI analysis for exploring the neuronal connectivity of the hippocampal formation in rats. Neurosci Res. 2012; 74: 248-255. doi: 10.1016/j.neures.2012.08.007 PMID: 22982343
35. Christie IN, Wells JA, Southern P, Marina N, Kasparov S, Gourine AV, et al. fMRI response to blue light delivery in the naïve brain: Implications for combined optogenetic fMRI studies. Neuroimage. 2012; 66: 634-641. doi: 10.1016/j.neuroimage.2012.10.074 PMID: 23128081
36. Berndt A, Yizhar O, Gunaydin LA, Hegemann P, Deisseroth K. Bi-stable neural state switches. Nat Neurosci. 2009; 12: 229-234. doi: 10.1038/nn.2247 PMID: 19079251
37. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 2005; 8: 1263-1268. doi: 10.1038/nn1525 PMID: 16116447
38. Van Zijl PCM, Hua J, Lu H. The BOLD post-stimulus undershoot, one of the most debated issues in fMRI. NeuroImage. 2012; 62: 1092-1102. doi: 10.1016/j.neuroimage.2012.01.029 PMID: 22248572
39. Shmuel A, Augath M, Oeltermann A, Logothetis NK. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci. 2006; 9: 569-577. doi: 10.1038/nn1675 PMID: 16547508
40. Weitz AJ, Fang Z, Lee HJ, Fisher RS, Smith WC, Choy M, et al. Optogenetic fMRI reveals distinct, frequency-dependent networks recruited by dorsal and intermediate hippocampus stimulations. Neuro-Image. 2015; 107: 229-241. doi: 10.1016/j.neuroimage.2014.10.039 PMID: 25462689
41. Nair G, Duong TQ. Echo-planar BOLD fMRI of mice on a narrow-bore 9.4 T magnet. Magn Reson Med. 2004; 52: 430-434. doi: 10.1002/mrm.20158 PMID: 15282829
42. Desai M, Kahn I, Knoblich U, Bernstein J, Atallah H, Yang A, et al. Mapping Brain Networks in Awake Mice Using Combined Optical Neural Control and fMRI. J Neurophysiol. 2011; 105: 1393-1405. doi: 10.1152/jn.00828.2010 PMID: 21160013
43. Grandjean J, Schroeter A, Batata I, Rudin M. Optimization of anesthesia protocol for resting-state fMRI in mice based on differential effects of anesthetics on functional connectivity patterns. Neuroimage. 2014; 102P2: 838-847. doi: 10.1016/j.neuroimage.2014.08.043 PMID: 25175535
44. Jonckers E, Delgado Y Palacios R, Shah D, Guglielmetti C, Verhoye M, Van der Linden A. Different anesthesia regimes modulate the functional connectivity outcome in mice. Magn Reson Med. 2013; 72: 1103-1112. doi: 10.1002/mrm.24990 PMID: 24285608
45. Sinclair MD. A review of the physiological effects of alpha2-agonists related to the clinical use of medetomidine in small animal practice. Can Vet J. 2003; 44: 885-897. PMID: 14664351
46. Weber R, Ramos-Cabrer P, Wiedermann D, van Camp N, Hoehn M. A fully noninvasive and robust experimental protocol for longitudinal fMRI studies in the rat. Neuroimage. 2006; 29: 1303-1310. doi: 10.1016/j.neuroimage.2005.08.028 PMID: 16223588
47. Takata N, Shinohara Y, Ohkura M, Mishima T, Nakai J, Hirase H. Imaging of Astrocytic Activity in Living Rodents. In: Weber B, Helmchen F, editors. Optical Imaging of Neocortical Dynamics. Springer Berlin/Heidelberg, in press; 2014. pp. 191-207.
48. Hara K, Harris RA. The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg. 2002; 94: 313-318, table of contents. PMID: 11812690
49. Vann SD, Aggleton JP, Maguire EA. What does the retrosplenial cortex do? Nat Rev Neurosci. 2009; 10: 792-802. doi: 10.1038/nrn2733 PMID: 19812579
50. Singewald GM, Rjabokon A, Singewald N, Ebner K. The Modulatory Role of the Lateral Septum on Neuroendocrine and Behavioral Stress Responses. Neuropsychopharmacology. 2011; 36: 793-804. doi: 10.1038/npp.2010.213 PMID: 21160468
51. Ranganath C, Ritchey M. Two cortical systems for memory-guided behaviour. Nat Rev Neurosci. 2012; 13: 713-726. doi: 10.1038/nrn3338 PMID: 22992647