Medial septal nucleus theta frequency deep brain stimulation improves spatial working memory after traumatic brain injury

Journal of Neurotrauma

Volumn 30, Issue 2, 2013, Pages 131-139

  Lee, Darrin J ^a   Gurkoff, Gene G ^a   Izadi, Ali ^a   Berman, Robert F ^a   Ekstrom, Arne D ^a   Muizelaar, J Paul ^a   Lyeth, Bruce G ^a   Shahlaie, Kiarash ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

deep brain stimulation; hippocampus; medial septal nucleus; TBI; theta oscillations

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; HIPPOCAMPUS THETA RHYTHM; LEARNING DISORDER; MALE; MAZE TEST; MEDIAL SEPTAL NUCLEUS; NEUROMODULATION; NONHUMAN; OSCILLATION; RAT; SEPTUM NUCLEUS; TRAUMATIC BRAIN INJURY; WORKING MEMORY;

ANIMALS; BRAIN INJURIES; DEEP BRAIN STIMULATION; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; RATS; RATS, SPRAGUE-DAWLEY; SEPTAL NUCLEI;

EID: 84872146864     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2646     Document Type: Article

References (56)

1. Slovarp, L., Azuma, T., and Lapointe, L. (2012). The effect of traumatic brain injury on sustained attention and working memory. Brain Inj. 26, 48-57.
2. Palacios, E.M., Sala-Llonch, R., Junque, C., Roig, T., Tormos, J.M., Bargallo, N., and Vendrell, P. (2012). White matter integrity related to functional working memory networks in traumatic brain injury. Neurology 78, 852-860.
3. Faul, M., Xu, L., Wald, M.M., and Coronado, V.G. (2010). Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002-2006. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control. CfDCa, NCfIPa C (eds). U.S. Department of Health and Human Services: Atlanta.
4. McAllister, T.W., Flashman, L.A., McDonald, B.C., and Saykin, A.J. (2006). Mechanisms of working memory dysfunction after mild and moderate TBI: evidence from functional MRI and neurogenetics. J. Neurotrauma 23, 1450-1467. (Pubitemid 46489605)
5. Laxton, A.W., Tang-Wai, D.F., McAndrews, M.P., Zumsteg, D., Wennberg, R., Keren, R., Wherrett, J., Naglie, G., Hamani, C., Smith, G.S., and Lozano, A.M. (2010). A phase I trial of deep brain stimulation of memory circuits in Alzheimer's disease. Ann. Neurol. 68, 521-534.
6. Suthana, N., Haneef, Z., Stern, J., Mukamel, R., Behnke, E., Knowlton, B., and Fried, I. (2012). Memory enhancement and deep-brain stimulation of the entorhinal area. N. Engl. J. Med. 366, 502-510.
7. Vertes, R.P. (2005). Hippocampal theta rhythm: a tag for short-term memory. Hippocampus 15, 923-935. (Pubitemid 41556422)
8. Buzsaki, G. (2005). Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827-840. (Pubitemid 41556413)
9. McNaughton, N., Ruan, M., and Woodnorth, M.-A. (2006). Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus 16, 1102-1110. (Pubitemid 46062834)
10. Mizumori, S.J., Perez, G.M., Alvarado, M.C., Barnes, C.A., and McNaughton, B.L. (1990). Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res. 528, 12-20. (Pubitemid 20292931)
11. Green, J.D., and Arduini, A.A. (1954). Hippocampal electrical activity in arousal. J. Neurophysiol. 17, 533-557.
12. Vanderwolf, C.H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418.
13. Wang, X.J. (2002). Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop. J. Neurophysiol. 87, 889-900.
14. McNaughton, B.L., and Barnes, C.A. (1977). Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. J. Comp. Neurol. 175, 439-454.
15. Sederberg, P.B., Kahana, M.J., Howard, M.W., Donner, E.J., and Madsen, J.R. (2003). Theta and gamma oscillations during encoding predict subsequent recall. J. Neurosci. 23, 10,809-10,814. (Pubitemid 37499687)
16. Addante, R.J., Watrous, A.J., Yonelinas, A.P., Ekstrom, A.D., and Ranganath, C. (2011). Prestimulus theta activity predicts correct source memory retrieval. Proc. Natl. Acad. Sci. U. S. A. 108, 10,702-10,707.
17. Landfield, P.W., McGaugh, J.L., and Tusa, R.J. (1972). Theta rhythm: a temporal correlate of memory storage processes in the rat. Science 175, 87-89.
18. Darling, R.D., Takatsuki, K., Griffin, A.L., and Berry, S.D. (2011). Eyeblink conditioning contingent on hippocampal theta enhances hippocampal and medial prefrontal responses. J. Neurophysiol. 105, 2213-2224.
19. Fedor, M., Berman, R.F., Muizelaar, J.P., and Lyeth, B.G. (2010). Hippocampal theta dysfunction after lateral fluid percussion injury. J. Neurotrauma 27, 1605-1615.
20. Eakin, K., and Miller, J.P. (2012). Mild traumatic brain injury is associated with impaired hippocampal spatiotemporal representation in the absence of histological changes. J. Neurotrauma 29, 1180-1187.
21. Dixon, C.E., Lyeth, B.G., Povlishock, J.T., Findling, R.L., Hamm, R.J., Marmarou, A., Young, H.F., and Hayes, R.L. (1987). A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119. (Pubitemid 17085024)
22. McIntosh, T.K., Vink, R., Noble, L., Yamakami, I., Fernyak, S., Soares, H., and Faden, A.L. (1989). Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233-244. (Pubitemid 19026758)
23. Barnes, C.A. (1979). Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93, 74-104. (Pubitemid 9140564)
24. Lawson, V.H., and Bland, B.H. (1993). The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: analysis by the intraseptal microinfusion of carbachol, atropine, and procaine. Exp. Neurol. 120, 132-144. (Pubitemid 23114037)
25. Vertes, R.P., and Kocsis, B. (1997). Brainstem-diencephalo- septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81, 893-926. (Pubitemid 27421757)
26. Delahunty, T.M., Jiang, J.Y., Gong, Q.Z., Black, R.T., and Lyeth, B.G. (1995). Differential consequences of lateral and central fluid percussion brain injury on receptor coupling in rat hippocampus. J. Neurotrauma 12, 1045-1057. (Pubitemid 26044668)
27. Lowenstein, D.H., Thomas, M.J., Smith, D.H., and McIntosh, T.K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12, 4846-4853.
28. Vertes, R.P., Albo, Z., and Viana, Di Prisco, G. (2001). Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez's circuit. Neuroscience 104, 619-625. (Pubitemid 32607415)
29. Kocsis, B., and Vertes, R.P. (1997). Phase relations of rhythmic neuronal firing in the supramammillary nucleus and mammillary body to the hippocampal theta activity in urethane anesthetized rats. Hippocampus 7, 204-214. (Pubitemid 27192402)
30. Colom, L.V., Christie, B.R., and Bland, B.H. (1988). Cingulate cell discharge patterns related to hippocampal EEG and their modulation by muscarinic and nicotinic agents. Brain Res. 460, 329-338.
31. Cortez, S.C., McIntosh, T.K., and Noble, L.J. (1989). Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res. 482, 271-282. (Pubitemid 19066539)
32. Conti, A.C., Raghupathi, R., Trojanowski, J.Q., and McIntosh, T.K. (1998). Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J. Neurosci. 18, 5663-5672. (Pubitemid 28341346)
33. Gorman, L.K., Fu, K., Hovda, D.A., Murray, M., and Traystman, R.J. (1996). Effects of traumatic brain injury on the cholinergic system in the rat. J. Neurotrauma 13, 457-463. (Pubitemid 26313524)
34. Shin, S.S., Bray, E.R., Zhang, C.Q., and Dixon, C.E. (2011). Traumatic brain injury reduces striatal tyrosine hydroxylase activity and potassium-evoked dopamine release in rats. Brain Res. 1369, 208-215.
35. Saatman, K.E., Graham, D.I., and McIntosh, T.K. (1998). The neuronal cytoskeleton is at risk after mild and moderate brain injury. J. Neurotrauma 15, 1047-1058. (Pubitemid 28560047)
36. Ekstrom, A.D., Caplan, J.B., Ho, E., Shattuck, K., Fried, I., and Kahana, M.J. (2005). Human hippocampal theta activity during virtual navigation. Hippocampus 15, 881-889. (Pubitemid 41556418)
37. Winson, J. (1974). Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr. Clin. Neurophysiol. 36, 291-301.
38. Nyhus, E., and Curran, T. (2010). Functional role of gamma and theta oscillations in episodic memory. Neurosci. Biobehav. Rev. 34, 1023-1035.
39. Jacobs, J., and Kahana, M.J. (2009). Neural representations of individual stimuli in humans revealed by gamma-band electrocorticographic activity. J. Neurosci. 29, 10,203-10,214.
40. Raghavachari, S., Kahana, M.J., Rizzuto, D.S., Caplan, J.B., Kirschen, M.P., Bourgeois, B., Madsen, J.R., and Lisman, J.E. (2001). Gating of human theta oscillations by a working memory task. J. Neurosci. 21, 3175-3183. (Pubitemid 32323499)
41. Lundqvist, M., Herman, P., and Lansner, A. (2011). Theta and gamma power increases and alpha/beta power decreases with memory load in an attractor network model. J. Cogn. Neurosci. 23, 3008-3020.
42. Takahashi, M., Lauwereyns, J., Sakurai, Y., and Tsukada, M. (2009). Behavioral state-dependent episodic representations in rat CA1 neuronal activity during spatial alternation. Cogn. Neurodyn. 3, 165-175.
43. Jensen, O., and Lisman, J.E. (1996). Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn. Mem. 3, 279-287. (Pubitemid 26357752)
44. Igarashi, J., Hayashi, H., and Tateno, K. (2007). Theta phase coding in a network model of the entorhinal cortex layer II with entorhinal-hippocampal loop connections. Cogn. Neurodyn. 1, 169-184.
45. Belluscio, M.A., Mizuseki, K., Schmidt, R., Kempter, R., and Buzsaki, G. (2012). Cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus. J. Neurosci. 32, 423-435.
46. Hallam, T.M., Floyd, C.L., Folkerts, M.M., Lee, L.L., Gong, Q.Z., Lyeth, B.G., Muizelaar, J.P., and Berman, R.F. (2004). Comparison of behavioral deficits and acute neuronal degeneration in rat lateral fluid percussion and weight-drop brain injury models. J, Neurotrauma 21, 521-539. (Pubitemid 38656750)
47. Lyeth, B.G., Jenkins, L.W., Hamm, R.J., Dixon, C.E., Phillips, L.L., Clifton, G.L., Young, H.F., and Hayes, R.L. (1990). Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Res. 526, 249-258. (Pubitemid 20307884)
48. Garcia-Panach, J., Lull, N., Lull, J.J., Ferri, J., Martinez, C., Sopena, P., Robles, M., Chirivella, J., and Noe, E. (2011). A voxel-based analysis of FDG-PET in traumatic brain injury: regional metabolism and relationship between the thalamus and cortical areas. J. Neurotrauma 28, 1707-1717.
49. Liu, Y.R., Cardamone, L., Hogan, R.E., Gregoire, M.C., Williams, J.P., Hicks, R.J., Binns, D., Koe, A., Jones, N.C., Myers, D.E., O'Brien, T.J., and Bouilleret, V. (2010). Progressive metabolic and structural cerebral perturbations after traumatic brain injury: an in vivo imaging study in the rat. J. Nucl. Med. 51, 1788-1795.
50. Thomas, S., Prins, M.L., Samii, M., and Hovda, D.A. (2000). Cerebral metabolic response to traumatic brain injury sustained early in development: a 2-deoxy-D-glucose autoradiographic study. J. Neurotrauma 17, 649-665.
51. Glenn, T.C., Kelly, D.F., Boscardin, W.J., McArthur, D.L., Vespa, P., Oertel, M., Hovda, D.A., Bergsneider, M., Hillered, L., and Martin, N.A. (2003). Energy dysfunction as a predictor of outcome after moderate or severe head injury, indices of oxygen, glucose, and lactate metabolism. J. Cereb. Blood Flow Metab. 23, 1239-1250. (Pubitemid 37229527)
52. Moore, A.H., Osteen, C.L., Chatziioannou, A.F., Hovda, D.A., and Cherry, S.R. (2000). Quantitative assessment of longitudinal metabolic changes in vivo after traumatic brain injury in the adult rat using FDG-microPET. J. Cereb. Blood Flow Metab. 20, 1492-1501.
53. Yamamoto, T., and Katayama, Y. (2005). Deep brain stimulation therapy for the vegetative state. Neuropsychol. Rehabil. 15, 406-413. (Pubitemid 41248346)
54. Yamamoto, T., Kobayashi, K., Kasai, M., Oshima, H., Fukaya, C., and Katayama, Y. (2005). DBS therapy for the vegetative state and minimally conscious state. Acta Neurochir. Suppl. 93, 101-104.
55. Schiff, N.D., Giacino, J.T., Kalmar, K., Victor, J.D., Baker, K., Gerber, M., Fritz, B., Eisenberg, B., Biondi, T., O'Connor, J., Kobylarz, E.J., Farris, S., Machado, A., McCagg, C., Plum, F., Fins, J.J., and Rezai, A.R. (2007). Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600-603. (Pubitemid 47206940)
56. Bricolo, A., Turazzi, S., and Feriotti, G. (1980). Prolonged posttraumatic unconsciousness: therapeutic assets and liabilities. J. Neurosurg. 52, 625-634.