Synchronized electrical stimulation of the rat medial forebrain bundle and perforant pathway generates an additive BOLD response in the nucleus accumbens and prefrontal cortex

NeuroImage

Volumn 77, Issue , 2013, Pages 14-25

  Krautwald, Karla ^a   Min, Hoon Ki ^b   Lee, Kendall H ^b   Angenstein, Frank ^a,c  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b MAYO CLINIC   (United States)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Dopamine; Electrochemistry; Electrophysiology; FMRI; Hippocampus; Nucleus accumbens; VTA

Indexed keywords

ANIMAL EXPERIMENT; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; BRAIN DEPTH STIMULATION; BRAIN REGION; CORTICAL SYNCHRONIZATION; DENTATE GYRUS; ENTORHINAL CORTEX; HIPPOCAMPUS; MALE; MEDIAL FOREBRAIN BUNDLE; NONHUMAN; NUCLEUS ACCUMBENS; PERFORANT NERVE TRACT; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SUBICULUM; SUBSTANTIA NIGRA; SUPERIOR COLLICULUS; VENTRAL TEGMENTUM; VENTROMEDIAL PREFRONTAL CORTEX;

ANIMALS; BRAIN MAPPING; ELECTRIC STIMULATION; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEDIAL FOREBRAIN BUNDLE; NUCLEUS ACCUMBENS; PERFORANT PATHWAY; PREFRONTAL CORTEX; RATS; RATS, WISTAR;

EID: 84876718199     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.03.046     Document Type: Article

References (39)

1. Agnesi F., Tye S.J., Bledsoe J.M., Griessenauer C.J., Kimble C.J., Sieck G.C., Bennet K.E., Garris P.A., Blaha C.D., Lee K.H. Wireless instantaneous neurotransmitter concentration system-based amperometric detection of dopamine, adenosine, and glutamate for intraoperative neurochemical monitoring. J. Neurosurg. 2009, 111:701-711.
2. Amaral D., Lavenex P. Hippocampal neuroanatomy. The Hippocampus Book 2007, 37-114. Oxford University Press, Oxford, New York. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
3. Angenstein F., Kammerer E., Niessen H.G., Frey J.U., Scheich H., Frey S. Frequency-dependent activation pattern in the rat hippocampus, a simultaneous electrophysiological and fMRI study. NeuroImage 2007, 38:150-163.
4. Angenstein F., Kammerer E., Scheich H. The BOLD response in the rat hippocampus depends rather on local processing of signals than on the input or output activity. A combined functional MRI and electrophysiological study. J. Neurosci. 2009, 29:2428-2439.
5. Beckstead R.M., Edwards S.B., Frankfurter A. A comparison of the intranigral distribution of nigrotectal neurons labeled with horseradish peroxidase in the monkey, cat, and rat. J. Neurosci. 1981, 1:121-125.
6. Berridge C.W., Stratford T.L., Foote S.L., Kelley A.E. Distribution of dopamine beta-hydroxylase-like immunoreactive fibers within the shell subregion of the nucleus accumbens. Synapse 1997, 27:230-241.
7. Bickford M.E., Hall W.C. The nigral projection to predorsal bundle cells in the superior colliculus of the rat. J. Comp. Neurol. 1992, 319:11-33.
8. Bledsoe J.M., Kimble C.J., Covey D.P., Blaha C.D., Agnesi F., Mohseni P., Whitlock S., Johnson D.M., Horne A., Bennet K.E., Lee K.H., Garris P.A. Development of the wireless instantaneous neurotransmitter concentration system for intraoperative neurochemical monitoring using fast-scan cyclic voltammetry. J. Neurosurg. 2009, 111:712-723.
9. Canals S., Beyerlein M., Murayama Y., Logothetis N.K. Electric stimulation fMRI of the perforant pathway to the rat hippocampus. Magn. Reson. Imaging 2008, 26:978-986.
10. Canals S., Beyerlein M., Merkle H., Logothetis N.K. Functional MRI evidence for LTP-induced neural network reorganization. Curr. Biol. 2009, 19:398-403.
11. Cebrian C., Parent A., Prensa L. Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat. J. Comp. Neurol. 2005, 492:349-369.
12. Cheer J.F., Heien M.L., Garris P.A., Carelli R.M., Wightman R.M. Simultaneous dopamine and single-unit recordings reveal accumbens GABAergic responses: implications for intracranial self-stimulation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19150-19155.
13. Choi J.K., Chen Y.I., Hamel E., Jenkins B.G. Brain hemodynamic changes mediated by dopamine receptors: role of the cerebral microvasculature in dopamine-mediated neurovascular coupling. NeuroImage 2006, 30:700-712.
14. Delfs J.M., Zhu Y., Druhan J.P., Aston-Jones G.S. Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: anterograde and retrograde tract-tracing studies in the rat. Brain Res. 1998, 806:127-140.
15. Edvinsson L., McCulloch J., Sharkey J. Vasomotor responses of cerebral arterioles in situ to putative dopamine receptor agonists. Br. J. Pharmacol. 1985, 85:403-410.
16. Gabriele M.L., Smoot J.E., Jiang H., Stein B.E., McHaffie J.G. Early establishment of adult-like nigrotectal architecture in the neonatal cat: a double-labeling study using carbocyanine dyes. Neuroscience 2006, 137:1309-1319.
17. Garbarg M., Barbin G., Feger J., Schwartz J.C. Histaminergic pathway in rat brain evidenced by lesions of the medial forebrain bundle. Science 1974, 186:833-835.
18. Groenewegen H.J., Wright C.I., Beijer A.V. The nucleus accumbens: gateway for limbic structures to reach the motor system?. Prog. Brain Res. 1996, 107:485-511.
19. Hashemi P., Dankoski E.C., Wood K.M., Ambrose R.E., Wightman R.M. In vivo electrochemical evidence for simultaneous 5-HT and histamine release in the rat substantia nigra pars reticulata following medial forebrain bundle stimulation. J. Neurochem. 2011, 118:749-759.
20. Helbing C., Werner G., Angenstein F. Variations in the temporal pattern of perforant pathway stimulation control the activity in the mesolimbic pathway. NeuroImage 2013, 64C:43-60.
21. Hennig J., Nauerth A., Friedburg H. RARE imaging: a fast imaging method for clinical MR. Magn. Reson. Med. 1986, 3:823-833.
22. Humphries M.D., Prescott T.J. The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. Prog. Neurobiol. 2010, 90:385-417.
23. Ingvar M., Lindvall O., Stenevi U. Apomorphine-induced changes in local cerebral blood flow in normal rats and after lesions of the dopaminergic nigrostriatal bundle. Brain Res. 1983, 262:259-265.
24. Joseph J.P., Boussaoud D. Role of the cat substantia nigra pars reticulata in eye and head movements. I. Neural activity. Exp. Brain Res. 1985, 57:286-296.
25. Kohler C., Swanson L.W., Haglund L., Wu J.Y. The cytoarchitecture, histochemistry and projections of the tuberomammillary nucleus in the rat. Neuroscience 1985, 16:85-110.
26. Mamounas L.A., Mullen C.A., O'Hearn E., Molliver M.E. Dual serotoninergic projections to forebrain in the rat: morphologically distinct 5-HT axon terminals exhibit differential vulnerability to neurotoxic amphetamine derivatives. J. Comp. Neurol. 1991, 314:558-586.
27. Miyazaki I., Asanuma M., Diaz-Corrales F.J., Miyoshi K., Ogawa N. Direct evidence for expression of dopamine receptors in astrocytes from basal ganglia. Brain Res. 2004, 1029:120-123.
28. Mogenson G.J., Jones D.L., Yim C.Y. From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 1980, 14:69-97.
29. Morrow T.J., Paulson P.E., Danneman P.J., Casey K.L. Regional changes in forebrain activation during the early and late phase of formalin nociception: analysis using cerebral blood flow in the rat. Pain 1998, 75:355-365.
30. Panula P., Pirvola U., Auvinen S., Airaksinen M.S. Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience 1989, 28:585-610.
31. Scarnati E., Campana E., Pacitti C. The functional role of the nucleus accumbens in the control of the substantia nigra: electrophysiological investigations in intact and striatum-globus pallidus lesioned rats. Brain Res. 1983, 265:249-257.
32. Sesack S.R., Grace A.A. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 2010, 35:27-47.
33. Shih Y.Y., Chen C.C., Shyu B.C., Lin Z.J., Chiang Y.C., Jaw F.S., Chen Y.Y., Chang C. A new scenario for negative functional magnetic resonance imaging signals: endogenous neurotransmission. J. Neurosci. 2009, 29:3036-3044.
34. Shih Y.Y., Wey H.Y., De La Garza B.H., Duong T.Q. Striatal and cortical BOLD, blood flow, blood volume, oxygen consumption, and glucose consumption changes in noxious forepaw electrical stimulation. J. Cereb. Blood Flow Metab. 2011, 31:832-841.
35. Somogyi P., Bolam J.P., Totterdell S., Smith A.D. Monosynaptic input from the nucleus accumbens-ventral striatum region to retrogradely labelled nigrostriatal neurones. Brain Res. 1981, 217:245-263.
36. Steffensen S.C., Svingos A.L., Pickel V.M., Henriksen S.J. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J. Neurosci. 1998, 18:8003-8015.
37. Thierry A.M., Gioanni Y., Degenetais E., Glowinski J. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 2000, 10:411-419.
38. Vertes R.P. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J. Comp. Neurol. 1991, 313:643-668.
39. Witter M.P. Connections of the subiculum of the rat: topography in relation to columnar and laminar organization. Behav. Brain Res. 2006, 174:251-264.