Deep brain stimulation in dementia-related disorders

Neuroscience and Biobehavioral Reviews

Volumn 37, Issue 10, 2013, Pages 2666-2675

  Hescham, Sarah ^a,d   Lim, Lee Wei ^c   Jahanshahi, Ali ^a,d   Blokland, Arjan ^b,d   Temel, Yasin ^a,d  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d European Graduate School of Neuroscience   (Netherlands)

Author keywords

Alzheimer's disease; Deep brain stimulation; Dementia; Entorhinal cortex; Fornix; Hippocampus; Limbic system; Memory; Neuroanatomy; Nucleus basalis of Meynert; Papez circuit

Indexed keywords

ALZHEIMER DISEASE; AMNESIA; AMYGDALOID NUCLEUS; BRAIN DEPTH STIMULATION; BRAIN FORNIX; BRAIN REGION; DEMENTIA; DENTATE GYRUS; ENTORHINAL CORTEX; HIPPOCAMPUS; HUMAN; LIMBIC CORTEX; LIMBIC SYSTEM; MEMORY DISORDER; MEYNERT BASAL NUCLEUS; MOSSY FIBER; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TASK PERFORMANCE; THALAMUS ANTERIOR NUCLEUS;

ALZHEIMER'S DISEASE; DEEP BRAIN STIMULATION; DEMENTIA; ENTORHINAL CORTEX; FORNIX; HIPPOCAMPUS; LIMBIC SYSTEM; MEMORY; NEUROANATOMY; NUCLEUS BASALIS OF MEYNERT; PAPEZ CIRCUIT;

ANIMALS; DEEP BRAIN STIMULATION; DEMENTIA; HUMANS;

EID: 84889632158     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2013.09.002     Document Type: Review

References (92)

1. Aggleton J., Brown M. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci. 1999, 22:425-444.
2. Aggleton J., Hunt P., Nagle S., Neave N. The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav. Brain Res. 1996, 81:189-198.
3. Aggleton J., Keith A., Sahgal A. Both fornix and anterior thalamic, but not mammillary, lesions disrupt delayed non-matching-to-position memory in rats. Behav. Brain Res. 1991, 44:151-161.
4. Aggleton J.P., Mishkin D.R.M. The origin, course, and termination of the hippocampothalamic projections in the macaque. J. Comp. Neurol. 1986, 243:409-421.
5. Aggleton J.P., O'Mara S.M., Vann S.D., Wright N.F., Tsanov M., Erichsen J.T. Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur. J. Neurosci. 2010, 31:2292-2307.
6. Andrade D.M., Zumsteg D., Hamani C., Hodaie M., Sarkissian S., Lozano A.M., Wennberg R.A. Long-term follow-up of patients with thalamic deep brain stimulation for epilepsy. Neurology 2006, 66:1571-1573.
7. Bartus R.T., Dean R.L., Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science 1982, 217:408-414.
8. Bentwich J., Dobronevsky E., Aichenbaum S., Shorer R., Peretz R., Khaigrekht M., Marton R., Rabey J. Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer's disease: a proof of concept study. J. Neural Transm. 2011, 118:463-471.
9. Bewernick B.H., Hurlemann R., Matusch A., Kayser S., Grubert C., Hadrysiewicz B., Axmacher N., Lemke M., Cooper-Mahkorn D., Cohen M.X., Brockmann H., Lenartz D., Sturm V., Schlaepfer T.E. Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol. Psychiatry 2010, 67:110-116.
10. Bigl V., Woolf N.J., Butcher L.L. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res. Bull. 1982, 8:727-749.
11. Boggio P.S., Ferrucci R., Rigonatti S.P., Covre P., Nitsche M., Pascual-Leone A., Fregni F. Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease. J. Neurol. Sci. 2006, 249:31-38.
12. Boggio P.S., Khoury L.P., Martins D.C.S., Martins O.E.M.S., de Macedo E.C., Fregni F. Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in Alzheimer disease. J. Neurol. Neurosurg. Psychiatry 2009, 80:444-447.
13. Boggio P.S., Valasek C.A., Campanhã C., Giglio A.C.A., Baptista N.I., Lapenta O.M., Fregni F. Non-invasive brain stimulation to assess and modulate neuroplasticity in Alzheimer's disease. Neuropsychol. Rehab. 2011, 21:703-716.
14. Bohnen N.I., Albin R.L. The cholinergic system and Parkinson disease. Behav. Brain Res. 2011, 221:564-573.
15. Broadbent N.J., Squire L.R., Clark R.E. Spatial memory, recognition memory, and the hippocampus. Proc. Natl. Acad. Sci. USA 2004, 101:14515-14520.
16. Brookmeyer R., Gray S., Kawas C. Projections of Alzheimer's disease in the United States and the public health impact of delaying disease onset. Am. J. Public Health 1998, 88:1337-1342.
17. Buckner R.L., Snyder A.Z., Shannon B.J., LaRossa G., Sachs R., Fotenos A.F., Sheline Y.I., Klunk W.E., Mathis C.A., Morris J.C., Mintun M.A. Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J. Neurosci. 2005, 25:7709-7717.
18. Célérier A., Ognard R., Decorte L., Beracochea D. Deficits of spatial and non-spatial memory and of auditory fear conditioning following anterior thalamic lesions in mice: comparison with chronic alcohol consumption. Eur. J. Neurosci. 2000, 12:2575-2584.
19. Cheney P.D., Giffin D.M., Van Acker G.M. Neural hijacking: action of high-frequency electrical stimulation on cortical circuits. Neuroscientist 2012, 19:434-441.
20. Clark R.E., Zola S.M., Squire L.R. Impaired recognition memory in rats after damage to the hippocampus. J. Neurosci. 2000, 20:8853-8860.
21. Cotelli M., Calabria M., Manenti R., Rosini S., Zanetti O., Cappa S.F., Miniussi C. Improved language performance in Alzheimer disease following brain stimulation. J. Neurol. Neurosurg. Psychiatry 2011, 82:794-797.
22. Cuello A.C., Bruno M.A., Allard S., Leon W., Iulita M.F. Cholinergic involvement in Alzheimer's disease. A link with NGF maturation and degradation. J. Mol. Neurosci. 2010, 40:230-235.
23. Denys D., Mantione M., Figee M., van den Munckhof P., Koerselman F., Westenberg H., Bosch A., Schuurman R. Deep brain stimulation of the nucleus accumbens for treatment-refractory obsessive-compulsive disorder. Arch. Gen. Psychiatry 2010, 67:1061-1068.
24. Dubois B., Feldman H.H., Jacova C., Cummings J.L., DeKosky S.T., Barberger-Gateau P., Delacourte A., Frisoni G., Fox N.C., Galasko D., Gauthier S., Hampel H., Jicha G.A., Meguro K., O'Brien J., Pasquier F., Robert P., Rossor M., Salloway S., Sarazin M., de Souza L.C., Stern Y., Visser P.J., Scheltens P. Revising the definition of Alzheimer's disease: a new lexicon. Lancet Neurol. 2010, 9:1118-1127.
25. Dumont J.R., Petrides M., Sziklas V. Fornix and retrosplenial contribution to a hippocampo-thalamic circuit underlying conditional learning. Behav. Brain Res. 2010, 209:13-20.
26. Eijkenboom M., Blokland A., van der Staay F.J. Modelling cognitive dysfunctions with bilateral injections of ibotenic acid into the rat entorhinal cortex. Neuroscience 2000, 101:27-39.
27. Ennaceur A., Neave N., Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp. Brain Res. 1997, 113:509-519.
28. Esiri M.M. The basis for behavioural disturbances in dementia. J. Neurol. Neurosurg. Psychiatry 1996, 61:127-130.
29. Fisher R., Salanova V., Witt T., Worth R., Henry T., Gross R., Oommen K., Osorio I., Nazzaro J., Labar D., Kaplitt M., Sperling M., Sandok E., Neal J., Handforth A., Stern J., DeSalles A., Chung S., Shetter A., Bergen D., Bakay R., Henderson J., French J., Baltuch G., Rosenfeld W., Youkilis A., Marks W., Garcia P., Barbaro N., Fountain N., Bazil C., Goodman R., McKhann G., Babu Krishnamurthy K., Papavassiliou S., Epstein C., Pollard J., Tonder L., Grebin J., Coffey R., Graves N. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia 2010, 51:899-908.
30. Fontaine D., Deudon A., Lemaire J.J., Razzouk M., Viau P., Darcourt J., Robert P. Symptomatic treatment of memory decline in Alzheimer's disease by deep brain stimulation: a feasibility study. J. Alzheimers Dis. 2013, 34:315-323.
31. Francis P.T., Palmer A.M., Snape M., Wilcock G.K. The cholinergic hypothesis of Alzheimer's disease: a review of progress. J. Neurol. Neurosurg. Psychiatry 1999, 66:137-147.
32. Fregni F., Boggio P., Nitsche M., Bermpohl F., Antal A., Feredoes E., Marcolin M., Rigonatti S., Silva M., Paulus W., Pascual-Leone A. Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp. Brain Res. 2005, 166:23-30.
33. Freund H.J., Kuhn J., Lenartz D., Mai J.K., Schnell T., Klosterkoetter J., Sturm V. Cognitive functions in a patient with Parkinson-dementia syndrome undergoing deep brain stimulation. Arch. Neurol. 2009, 66:781-785.
34. Gaskin S., Tremblay A., Mumby D.G. Retrograde and anterograde object recognition in rats with hippocampal lesions. Hippocampus 2003, 13:962-969.
35. Gemmell C., O'Mara S.M. Plasticity in the projection from the anterior thalamic nuclei to the anterior cingulate cortex in the rat in vivo: paired-pulse facilitation, long-term potentiation and short-term depression. Neuroscience 2002, 109:401-406.
36. Halgren E., Wilson C.L., Stapleton J.M. Human medial temporal-lobe stimulation disrupts both formation and retrieval of recent memories. Brain Cogn. 1985, 4:287-295.
37. Hamani C., Dubiela F.P., Soares J.C.K., Shin D., Bittencourt S., Covolan L., Carlen P.L., Laxton A.W., Hodaie M., Stone S.S.D., Ha Y., Hutchison W.D., Lozano A.M., Mello L.E., Oliveira M.G.M. Anterior thalamus deep brain stimulation at high current impairs memory in rats. Exp. Neurol. 2010, 225:154-162.
38. Hamani C., McAndrews M.P., Cohn M., Oh M., Zumsteg D., Shapiro C.M., Wennberg R.A., Lozano A.M. Memory enhancement induced by hypothalamic/fornix deep brain stimulation. Ann. Neurol. 2008, 63:119-123.
39. Hamani C., Stone S.S., Garten A., Lozano A.M., Winocur G. Memory rescue and enhanced neurogenesis following electrical stimulation of the anterior thalamus in rats treated with corticosterone. Exp. Neurol. 2011, 232:100-104.
40. Hamani C., Temel Y. Deep brain stimulation for psychiatric disease: contributions and validity of animal models. Sci. Transl. Med. 2012, 4:142rv148.
41. Hardenacke K., Kuhn J., Lenartz D., Maarouf M., Mai J., Bartsch C., Freund H., Sturm V. Stimulate or degenerate deep brain stimulation of the nucleus basalis Meynert in Alzheimer's dementia. World Neurosurg. 2013, in press.
42. Harnack D., Meissner W., Jira J.A., Winter C., Morgenstern R., Kupsch A. Placebo-controlled chronic high-frequency stimulation of the subthalamic nucleus preserves dopaminergic nigral neurons in a rat model of progressive Parkinsonism. Exp. Neurol. 2008, 210:257-260.
43. Hedberg T.G., Stanton P.K. Long-term potentiation and depression of synaptic transmission in rat posterior cingulate cortex. Brain Res. 1995, 670:181-196.
44. Hescham S., Lim L.W., Jahanshahi A., Steinbusch H.W., Prickaerts J., Blokland A., Temel Y. Deep brain stimulation of the forniceal area enhances memory functions in experimental dementia: the role of stimulation parameters. Brain Stimul. 2013, 6:72-77.
45. Hotta H., Kagitani F., Kondo M., Uchida S. Basal forebrain stimulation induces NGF secretion in ipsilateral parietal cortex via nicotinic receptor activation in adult, but not aged rats. Neurosci. Res. 2009, 63:122-128.
46. Houeto J.L., Karachi C., Mallet L., Pillon B., Yelnik J., Mesnage V., Welter M.L., Navarro S., Pelissolo A., Damier P., Pidoux B., Dormont D., Cornu P., Agid Y. Tourette's syndrome and deep brain stimulation. J. Neurol. Neurosurg. Psychiatry 2005, 76:992-995.
47. Köhler S., Paus T., Buckner R.L., Milner B. Effects of left inferior prefrontal stimulation on episodic memory formation: a two-stage fMRI-rTMS study. J. Cogn. Neurosci. 2004, 16:178-188.
48. Lacruz M.E., Valentin A., Seoane J.J., Morris R.G., Selway R.P., Alarcon G. Single pulse electrical stimulation of the hippocampus is sufficient to impair human episodic memory. Neuroscience 2010, 170:623-632.
49. Lacruz M.E., Valentín A., Seoane J.J.G., Morris R.G., Selway R.P., Alarcón G. Single pulse electrical stimulation of the hippocampus is sufficient to impair human episodic memory. Neuroscience 2010, 170:623-632.
50. 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., Lozano A.M. A phase I trial of deep brain stimulation of memory circuits in Alzheimer's disease. Ann. Neurol. 2010, 68:521-534.
51. Lobo A., Launer L.J., Fratiglioni L., Andersen K., Di Carlo A., Breteler M.M., Copeland J.R., Dartigues J.F., Jagger C., Martinez-Lage J., Soininen H., Hofman A. Prevalence of dementia and major subtypes in Europe: a collaborative study of population-based cohorts. Neurologic diseases in the elderly research group. Neurology 2000, 54:S4-S9.
52. 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.
53. Luber B., Kinnunen L.H., Rakitin B.C., Ellsasser R., Stern Y., Lisanby S.H. Facilitation of performance in a working memory task with rTMS stimulation of the precuneus: frequency- and time-dependent effects. Brain Res. 2007, 1128:120-129.
54. Maesawa S., Kaneoke Y., Kajita Y., Usui N., Misawa N., Nakayama A., Yoshida J. Long-term stimulation of the subthalamic nucleus in hemiparkinsonian rats: neuroprotection of dopaminergic neurons. J. Neurosurg. 2004, 100:679-687.
55. Mair R., Burk J., Porter M. Impairment of radial maze delayed nonmatching after lesions of anterior thalamus and parahippocampal cortex. Behav. Neurosci. 2003, 117:596-605.
56. Malone D.A., Dougherty D.D., Rezai A.R., Carpenter L.L., Friehs G.M., Eskandar E.N., Rauch S.L., Rasmussen S.A., Machado A.G., Kubu C.S., Tyrka A.R., Price L.H., Stypulkowski P.H., Giftakis J.E., Rise M.T., Malloy P.F., Salloway S.P., Greenberg B.D. Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol. Psychiatry 2009, 65:267-275.
57. Megías M., Emri Z., Freund T.F., Gulyás A.I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 2001, 102:527-540.
58. Moser M.B., Moser E.I., Forrest E., Andersen P., Morris R.G. Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. USA 1995, 92:9697-9701.
59. Mu Y., Gage F.H. Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol. Neurodegener. 2011, 6:85.
60. Mumby D.G., Piterkin P., Lecluse V., Lehmann H. Perirhinal cortex damage and anterograde object-recognition in rats after long retention intervals. Behav. Brain Res. 2007, 185:82-87.
61. Nandi D., Jenkinson N., Stein J., Aziz T. The pedunculopontine nucleus in Parkinson's disease: primate studies. Br. J. Neurosurg. 2008, 22(Suppl. 1):S4-S8.
62. Neave N., Lloyd S., Sahgal A., Aggleton J.P. Lack of effect of lesions in the anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat. Behav. Brain Res. 1994, 65:89-101.
63. Oswald C., Good M. The effects of combined lesions of the subicular complex and the entorhinal cortex on two forms of spatial navigation in the water maze. Behav. Neurosci. 2000, 114:211-217.
64. Parron C., Poucet B., Save E. Entorhinal cortex lesions impair the use of distal but not proximal landmarks during place navigation in the rat. Behav. Brain Res. 2004, 154:345-352.
65. Parron C., Save E. Comparison of the effects of entorhinal and retrosplenial cortical lesions on habituation, reaction to spatial and non-spatial changes during object exploration in the rat. Neurobiol. Learn. Mem. 2004, 82:1-11.
66. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998.
67. Plassman B.L., Langa K.M., Fisher G.G., Heeringa S.G., Weir D.R., Ofstedal M.B., Burke J.R., Hurd M.D., Potter G.G., Rodgers W.L., Steffens D.C., Willis R.J., Wallace R.B. Prevalence of dementia in the United States: the aging, demographics, and memory study. Neuroepidemiology 2007, 29:125-132.
68. Qaseem A., Snow V., Cross J.T., Forciea M.A., Hopkins R., Shekelle P., Adelman A., Mehr D., Schellhase K., Campos-Outcalt D., Santaguida P., Owens D.K., American College of Physicians/American Academy of Family Physicians Panel on Dementia. Current pharmacologic treatment of dementia: a clinical practice guideline from the American College of Physicians and the American Academy of Family Physicians. Ann. Intern. Med. 2008, 148:370-378.
69. Ranck J.B. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 1975, 98:417-440.
70. Revett T.J., Baker G.B., Jhamandas J., Kar S. Glutamate system, amyloid ss peptides and tau protein: functional interrelationships and relevance to Alzheimer disease pathology. J. Psychiatry Neurosci. 2012, 37:110190.
71. Rothblat L., Vnek N., Gleason T., Kromer L. Role of the parahippocampal region in spatial and non-spatial memory: effects of parahippocampal lesions on rewarded alternation and concurrent object discrimination learning in the rat. Behav. Brain Res. 1992, 55:93-100.
72. Santín L., Rubio S., Begega A., Arias J. Effects of mammillary body lesions on spatial reference and working memory tasks. Behav. Brain Res. 1998, 102:137-150.
73. Savica R., Stead M., Mack K.J., Lee K.H., Klassen B.T. Deep brain stimulation in Tourette syndrome: a description of 3 patients with excellent outcome. Mayo Clinic Proc. 2012, 87:59-62.
74. Smith G.S., Laxton A.W., Tang-Wai D.F., McAndrews M.P., Diaconescu A.O., Workman C.I., Lozano A.M. Increased cerebral metabolism after 1 year of deep brain stimulation in Alzheimer disease increased cerebral metabolism after 1 year of DBS. Arch. Neurol. 2012, 1-8.
75. Stone S.S.D., Teixeira C.M., DeVito L.M., Zaslavsky K., Josselyn S.A., Lozano A.M., Frankland P.W. Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J. Neurosci. 2011, 31:13469-13484.
76. Suthana N., Haneef Z., Stern J., Mukamel R., Behnke E., Knowlton B., Fried I. Memory enhancement and deep-brain stimulation of the entorhinal area. New Engl. J. Med. 2012, 366:502-510.
77. Tan S., Vlamings R., Lim L., Sesia T., Janssen M.L., Steinbusch H.W., Visser-Vandewalle V., Temel Y. Experimental deep brain stimulation in animal models. Neurosurgery 2010, 67:1073-1079. (discussion 1080).
78. Temel Y., Visser-Vandewalle V. Targets for deep brain stimulation in Parkinson's disease. Exp. Opin. Ther. Targets 2006, 10:355-362.
79. Temel Y., Visser-Vandewalle V., Kaplan S., Kozan R., Daemen M.A., Blokland A., Schmitz C., Steinbusch H.W. Protection of nigral cell death by bilateral subthalamic nucleus stimulation. Brain Res. 2006, 1120:100-105.
80. Thies W., Bleiler L. 2011 Alzheimer's disease facts and figures. Alzheimer's Dement. J. Alzheimer's Assoc. 2011, 7:208-244.
81. Tiwari V., Patel A.B. Impaired glutamatergic and GABAergic function at early age in AbetaPPswe-PS1dE9 mice: implications for Alzheimer's disease. J. Alzheimers Dis. 2012, 28:765-769.
82. Toda H., Hamani C., Fawcett A.P., Hutchison W.D., Lozano A.M. The regulation of adult rodent hippocampal neurogenesis by deep brain stimulation. J. Neurosurg. 2008, 108:132-138.
83. Trillo L., Das D., Hsieh W., Medina B., Moghadam S., Lin B., Dang V., Sanchez M.M., De Miguel Z., Ashford J.W., Salehi A. Ascending monoaminergic systems alterations in Alzheimer's disease. Translating basic science into clinical care. Neurosci. Biobehav. Rev. 2013, 37:1363-1379.
84. Tsivilis D., Vann S.D., Denby C., Roberts N., Mayes A.R., Montaldi D., Aggleton J.P. A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat. Neurosci. 2008, 11:834-842.
85. Turnbull I.M., McGeer P.L., Beattie L., Calne D., Pate B. Stimulation of the basal nucleus of Meynert in senile dementia of Alzheimer's type. A preliminary report. Appl. Neurophysiol. 1985, 48:216-221.
86. Vann S.D., Honey R.C., Aggleton J.P. Lesions of the mammillothalamic tract impair the acquisition of spatial but not nonspatial contextual conditional discriminations. Eur. J. Neurosci. 2003, 18:2413-2416.
87. Voon V., Krack P., Lang A.E., Lozano A.M., Dujardin K., Schupbach M., D'Ambrosia J., Thobois S., Tamma F., Herzog J., Speelman J.D., Samanta J., Kubu C., Rossignol H., Poon Y.Y., Saint-Cyr J.A., Ardouin C., Moro E. A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson's disease. Brain 2008, 131:2720-2728.
88. Wallace B.A., Ashkan K., Heise C.E., Foote K.D., Torres N., Mitrofanis J., Benabid A.L. Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP-treated monkeys. Brain 2007, 130:2129-2145.
89. Warburton E.C., Baird A.L., Morgan A., Muir J.L., Aggleton J.P. Disconnecting hippocampal projections to the anterior thalamus produces deficits on tests of spatial memory in rats. Eur. J. Neurosci. 2000, 12:1714-1726.
90. Whishaw I., Cassel J., Jarrad L. Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J. Neurosci. 1995, 15:5779-5788.
91. Wichmann T., DeLong M.R. Deep brain stimulation for neurologic and neuropsychiatric disorders. Neuron 2006, 52:197-204.
92. Witter M.P., Naber P.A., van Haeften T., Machielsen W.C., Rombouts S.A., Barkhof F., Scheltens P., Lopes da Silva F.H. Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 2000, 10:398-410.