Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-29T17:06:09.376Z Has data issue: false hasContentIssue false

Impact of deep brain stimulation of the ventral anterior limb of the internal capsule on cognition in depression

Published online by Cambridge University Press:  09 February 2017

I. O. Bergfeld*
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Amsterdam Brain and Cognition, Amsterdam, The Netherlands
M. Mantione
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
M. L. C. Hoogendoorn
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
H. G. Ruhé
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Department of Psychiatry, Mood and Anxiety Disorders, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands
F. Horst
Affiliation:
Department of Psychiatry, ETZ, location Elisabeth, Tilburg, The Netherlands
P. Notten
Affiliation:
Department of Psychiatry, ETZ, location Elisabeth, Tilburg, The Netherlands
J. van Laarhoven
Affiliation:
Department of Psychiatry, ETZ, location Elisabeth, Tilburg, The Netherlands
P. van den Munckhof
Affiliation:
Department of Neurosurgery, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
G. Beute
Affiliation:
Department of Neurosurgery, ETZ, location Elisabeth, Tilburg, The Netherlands
P. R. Schuurman
Affiliation:
Department of Neurosurgery, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
D. Denys*
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Amsterdam Brain and Cognition, Amsterdam, The Netherlands Netherlands Institute for Neurosciences, an Institute of the Royal Dutch Academy of Science, Amsterdam, The Netherlands
*
*Address for correspondence: I. Bergfeld, M.Sc. and D. Denys, M.D. Ph.D., Department of Psychiatry, Academic Medical Center, PO Box 22660, 1100 DD Amsterdam, The Netherlands. (Email: [email protected]) [I. O. B.] (Email [email protected]) [D. D.]
*Address for correspondence: I. Bergfeld, M.Sc. and D. Denys, M.D. Ph.D., Department of Psychiatry, Academic Medical Center, PO Box 22660, 1100 DD Amsterdam, The Netherlands. (Email: [email protected]) [I. O. B.] (Email [email protected]) [D. D.]

Abstract

Background

Preliminary studies report no negative and a possible positive impact of deep brain stimulation (DBS) on cognition of patients with treatment-resistant depression (TRD). However, these studies neither controlled for practice effects nor compared active with sham stimulation.

Method

To address these limitations, we compared 25 TRD patients, who underwent DBS of the ventral anterior limb of the internal capsule (vALIC), with 21 healthy controls (HCs) matched on gender, age and education level. Both groups did subtests of the Cambridge Neuropsychological Test Automated Battery assessing verbal and visuospatial memory, attention, cognitive flexibility, psychomotor functioning, planning and object naming. TRD patients were tested 3 weeks prior to DBS surgery (baseline), 3 weeks following surgery (T1) and following 52 weeks of DBS optimization (T2). HCs were tested at baseline, 6 weeks following baseline (T1) and 20–24 weeks following baseline (T2). Subsequently, TRD patients entered a randomized, double-blind crossover phase, in which they were tested in an active and a sham stimulation phase.

Results

TRD patients did not improve on a test of immediate verbal recognition from baseline to T1, whereas HCs did (group x time: p = 0.001). Both TRD patients and HCs improved over sessions on tests measuring delayed verbal recall, visuospatial memory, planning and object naming (all p < 0.01). Active and sham stimulation did not have an impact on any of the tests differentially.

Conclusions

vALIC DBS neither has a lasting positive nor negative impact on cognition in TRD patients. DBS surgery might have a temporary negative effect on verbal memory.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ashton, CH (2002). Benzodiazepines: How they Work and How to Withdraw (benzo.org.uk).Google Scholar
Baune, BT, Renger, L (2014). Pharmacological and non-pharmacological interventions to improve cognitive dysfunction and functional ability in clinical depression – a systematic review. Psychiatry Research 219, 2550.Google Scholar
Bergfeld, IO, Mantione, M, Hoogendoorn, MLC, Denys, D (2013). Cognitive functioning in psychiatric disorders following deep brain stimulation. Brain Stimulation 6, 532537.CrossRefGoogle ScholarPubMed
Bergfeld, IO, Mantione, M, Hoogendoorn, MLC, Ruhé, HG, Notten, P, van Laarhoven, J, Visser, I, Figee, M, de Kwaasteniet, BP, Horst, F, Schene, AH, van den Munckhof, P, Beute, G, Schuurman, R, Denys, D (2016). Deep brain stimulation of the ventral anterior limb of the internal capsule for treatment-resistant depression: a randomized clinical trial. JAMA Psychiatry 73, 456464.Google Scholar
Bewernick, BH, Kayser, S, Sturm, V, Schlaepfer, TE (2012). Long-term effects of nucleus accumbens deep brain stimulation in treatment-resistant depression: evidence for sustained efficacy. Neuropsychopharmacology 37, 19751985.CrossRefGoogle ScholarPubMed
Bogod, NM, Sinden, M, Woo, C, Defreitas, VG, Torres, IJ, Howard, AK, Ilcewicz-Klimek, MI, Honey, CR, Yatham, LN, Lam, RW (2014). Long-term neuropsychological safety of subgenual cingulate gyrus deep brain stimulation for treatment-resistant depression. Journal of Neuropsychiatry and Clinical Neurosciences 26, 126133.Google Scholar
Brocker, DT, Grill, WM (2013). Principles of electrical stimulation of neural tissue. Handbook of Clinical Neurology 116, 318.CrossRefGoogle ScholarPubMed
Calamia, M, Markon, K, Tranel, D (2012). Scoring higher the second time around: meta-analyses of practice effects in neuropsychological assessment. Clinical Neuropsychologist 26, 543570.Google Scholar
Dougherty, DD, Rezai, AR, Carpenter, LL, Howland, RH, Bhati, MT, O'Reardon, JP, Eskandar, EN, Baltuch, GH, Machado, AD, Kondziolka, D, Cusin, C, Evans, KC, Price, LH, Jacobs, K, Pandya, M, Denko, T, Tyrka, AR, Brelje, T, Deckersbach, T, Kubu, C, Malone, DA Jr. (2015). A randomized sham-controlled trial of deep brain stimulation of the ventral capsule/ventral striatum for chronic treatment-resistant depression. Biological Psychiatry 78, 240248.Google Scholar
Douglas, KM, Porter, RJ (2009). Longitudinal assessment of neuropsychological function in major depression. Australian and New Zealand Journal of Psychiatry 43, 11051117.CrossRefGoogle ScholarPubMed
Eshel, N, Roiser, JP (2010). Reward and punishment processing in depression. Biological Psychiatry 68, 118124.Google Scholar
Figee, M, Luigjes, J, Smolders, R, Valencia-Alfonso, C-E, van Wingen, G, de Kwaasteniet, B, Mantione, M, Ooms, P, de Koning, P, Vulink, N, Levar, N, Droge, L, van den Munckhof, P, Schuurman, PR, Nederveen, A, van den Brink, W, Mazaheri, A, Vink, M, Denys, D (2013). Deep brain stimulation restores frontostriatal network activity in obsessive–compulsive disorder. Nature Neuroscience 16, 386387.Google Scholar
Grubert, C, Hurlemann, R, Bewernick, BH, Kayser, S, Hadrysiewicz, B, Axmacher, N, Sturm, V, Schlaepfer, TE (2011). Neuropsychological safety of nucleus accumbens deep brain stimulation for major depression: effects of 12-month stimulation World Journal of Biological Psychiatry 12, 516527.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
Holtzheimer, PE, Kelley, ME, Gross, RE, Filkowski, MM, Garlow, SJ, Barrocas, A, Wint, D, Craighead, MC, Kozarsky, J, Chismar, R, Moreines, JL, Mewes, K, Posse, PR, Gutman, DA, Mayberg, HS (2012). Subcallosal cingulate deep brain stimulation for treatment-resistant unipolar and bipolar depression. Archives of General Psychiatry 69, 150158.Google Scholar
IBM Corp. (2013). IBM SPSS Statistics for Windows (version 22.0) . IBM Corp.: Armonk, NY.Google Scholar
Kubu, CS, Malone, DA, Chelune, G, Malloy, P, Rezai, AR, Frazier, T, MacHado, A, Rasmussen, S, Friehs, G, Greenberg, BD (2013). Neuropsychological outcome after deep brain stimulation in the ventral capsule/ventral striatum for highly refractory obsessive–compulsive disorder or major depression. Stereotactic and Functional Neurosurgery 91, 374378.Google Scholar
Lehman, JF, Greenberg, BD, McIntyre, CC, Rasmussen, SA, Haber, SN (2011). Rules ventral prefrontal cortical axons use to reach their targets: implications for diffusion tensor imaging tractography and deep brain stimulation for psychiatric illness. Journal of Neuroscience 31, 1039210402.Google Scholar
Lozano, AM, Giacobbe, P, Hamani, C, Rizvi, SJ, Kennedy, SH, Kolivakis, TT, Debonnel, G, Sadikot, AF, Lam, RW, Howard, AK, Ilcewicz-Klimek, M, Honey, CR, Mayberg, HS (2012). A multicenter pilot study of subcallosal cingulate area deep brain stimulation for treatment-resistant depression. Journal of Neurosurgery 116, 315322.Google Scholar
Lozano, AM, Mayberg, HS, Giacobbe, P, Hamani, C, Craddock, RC, Kennedy, SH (2008). Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biological Psychiatry 64, 461467.CrossRefGoogle ScholarPubMed
Malone, DA, Dougherty, DD, Rezai, AR, Carpenter, LL, Friehs, GM, Eskandar, EN, Rauch, SL, Rasmussen, SA, Machado, AG, Kubu, CS, Tyrka, AR, Price, LH, Stypulkowski, PH, Giftakis, JE, Rise, MT, Malloy, PF, Salloway, SP, Greenberg, BD (2009). Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biological Psychiatry 65, 267275.CrossRefGoogle ScholarPubMed
McNeely, HE, Mayberg, HS, Lozano, AM, Kennedy, SH (2008). Neuropsychological impact of Cg25 deep brain stimulation for treatment-resistant depression: preliminary results over 12 months. Journal of Nervous and Mental Disease 196, 405410.Google Scholar
Moreines, JL, McClintock, SM, Kelley, ME, Holtzheimer, PE, Mayberg, HS (2014). Neuropsychological function before and after subcallosal cingulate deep brain stimulation in patients with treatment-resistant depression. Depression and Anxiety 31, 690698.Google Scholar
Puigdemont, D, Pérez-Egea, R, Portella, MJ, Molet, J, de Diego-Adeliño, J, Gironell, A, Radua, J, Gómez-Anson, B, Rodríguez, R, Serra, M, de Quintana, C, Artigas, F, Álvarez, E, Pérez, V (2012). Deep brain stimulation of the subcallosal cingulate gyrus: further evidence in treatment-resistant major depression. International Journal of Neuropsychopharmacology 15, 121133.CrossRefGoogle ScholarPubMed
Puigdemont, D, Portella, M, Pérez-Egea, R, Molet, J, Gironell, A, de Diego-Adeliño, J, Martín, A, Rodríguez, R, Àlvarez, E, Artigas, F, Pérez, V (2015). A randomized double-blind crossover trial of deep brain stimulation of the subcallosal cingulate gyrus in patients with treatment-resistant depression: a pilot study of relapse prevention. Journal of Psychiatry and Neuroscience 40, 224231.Google Scholar
Rock, PL, Roiser, JP, Riedel, WJ, Blackwell, AD (2014). Cognitive impairment in depression: a systematic review and meta-analysis. Psychological Medicine 44, 20292040.Google Scholar
Rosenblat, JD, Kakar, R, McIntyre, RS (2015). The cognitive effects of antidepressants in major depressive disorder: a systematic review and meta-analysis of randomized clinical trials. International Journal of Neuropsychopharmacology 19, pyv082.Google Scholar
Russo, SJ, Nestler, EJ (2013). The brain reward circuitry in mood disorders. Nature Reviews Neuroscience 14, 609625.CrossRefGoogle ScholarPubMed
Schlaepfer, TE, Bewernick, BH (2013). Deep brain stimulation for major depression. Handbook of Clinical Neurology 116, 235243.Google Scholar
Schlaepfer, TE, Bewernick, BH, Kayser, S, Mädler, B, Coenen, VA (2013). Rapid effects of deep brain stimulation for treatment-resistant major depression. Biological Psychiatry 73, 12041212.Google Scholar
Serra-Blasco, M, de Vita, S, Rodriguez, MR, de Diego-Adelino, J, Puigdemont, D, Martin-Blanco, A, Perez-Egea, R, Molet, J, Alvarez, E, Perez, V, Portella, MJ, Rodríguez, MR, de Diego-Adeliño, J, Puigdemont, D, Martín-Blanco, A, Pérez-Egea, R, Molet, J, Álvarez, E, Pérez, V, Portella, MJ (2015). Cognitive functioning after deep brain stimulation in subcallosal cingulate gyrus for treatment-resistant depression: an exploratory study. Psychiatry Research 225, 341346.Google Scholar
Tannenbaum, C, Paquette, A, Hilmer, S, Holroyd-Leduc, J, Carnahan, R (2012). A systematic review of amnestic and non-amnestic mild cognitive impairment induced by anticholinergic, antihistamine, GABAergic and opioid drugs. Drugs and Aging 29, 639658.Google Scholar
United Nations Educational, Scientific and Cultural Organization (UNESCO) (2011). International Standard Classification of Education: ISCED 2011 (http://www.uis.unesco.org/Education/Documents/isced-2011-en.pdf).Google Scholar
Veiel, HO (1997). A preliminary profile of neuropsychological deficits associated with major depression. Journal of Clinical and Experimental Neuropsychology 19, 587603.CrossRefGoogle ScholarPubMed
Supplementary material: File

Bergfeld supplementary material

Table S1

Download Bergfeld supplementary material(File)
File 48.1 KB