Deep brain stimulation for aggressiveness: long-term follow-up and tractography study of the stimulated brain areas

View More View Less
  • 1 Departments of Neurosurgery,
  • 2 Neuroradiology, and
  • 3 Clinical Neurophysiology, University Hospital La Princesa, Madrid;
  • 4 Department of Neuroradiology, Clínica Anderson, Madrid; and
  • 5 Department of Psychiatry, University Hospital La Princesa, Madrid, Spain
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

OBJECTIVE

Initial studies applying deep brain stimulation (DBS) of the posteromedial hypothalamus (PMH) to patients with pathological aggressiveness have yielded encouraging results. However, the anatomical structures involved in its therapeutic effect have not been precisely identified. The authors’ objective was to describe the long-term outcome in their 7-patient series, and the tractography analysis of the volumes of tissue activated in 2 of the responders.

METHODS

This was a retrospective study of 7 subjects with pathological aggressiveness. The findings on MRI with diffusion tensor imaging (DTI) in 2 of the responders were analyzed. The authors generated volumes of tissue activated according to the parameters used, and selected those volumes as regions of interest to delineate the tracts affected by stimulation.

RESULTS

The series consisted of 5 men and 2 women. Of the 7 patients, 5 significantly improved with stimulation. The PMH, ventral tegmental area, dorsal longitudinal fasciculus, and medial forebrain bundle seem to be involved in the stimulation field.

CONCLUSIONS

In this series, 5 of 7 medication-resistant patients with severe aggressiveness who were treated with bilateral PMH DBS showed a significant long-lasting improvement. The PMH, ventral tegmental area, dorsal longitudinal fasciculus, and medial forebrain bundle seem to be in the stimulation field and might be responsible for the therapeutic effect of DBS.

ABBREVIATIONS DBS = deep brain stimulation; DLF = dorsal longitudinal fasciculus; DTI = diffusion tensor imaging; EEG = electroencephalography; FOV = field of view; ICAP = Inventory for Client and Agency Planning; MCP = midcommissural point; MFB = medial forebrain bundle; OCD = obsessive-compulsive disorder; PMH = posteromedial hypothalamus; VEEG = video EEG; VTa = ventral tegmental area.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Correspondence Cristina V. Torres: University Hospital La Princesa, Madrid, Spain. cristinatorresdiaz@yahoo.es.

INCLUDE WHEN CITING Published online February 7, 2020; DOI: 10.3171/2019.11.JNS192608.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • 1

    Akram H, Miller S, Lagrata S, Hyam J, Jahanshahi M, Hariz M, : Ventral tegmental area deep brain stimulation for refractory chronic cluster headache. Neurology 86:16761682, 2016

    • Search Google Scholar
    • Export Citation
  • 2

    Andersen R: Cognitive changes after amygdalotomy. Neuropsychologia 16:439451, 1978

  • 3

    Astrom M, Diczfalusy E, Martens H, Wardell K: Relationship between neural activation and electric field distribution during deep brain stimulation. IEEE Trans Biomed Eng 62:664672, 2015

    • Search Google Scholar
    • Export Citation
  • 4

    Azmitia EC, Segal M: An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641667, 1978

    • Search Google Scholar
    • Export Citation
  • 5

    Balasubramaniam V, Kanaka TS: Amygdalotomy and hypothalamotomy - a comparative study. Confin Neurol 37:195201, 1975

  • 6

    Benedetti-Isaac JC, Torres-Zambrano M, Vargas-Toscano A, Perea-Castro E, Alcalá-Cerra G, Furlanetti LL, : Seizure frequency reduction after posteromedial hypothalamus deep brain stimulation in drug-resistant epilepsy associated with intractable aggressive behavior. Epilepsia 56:11521161, 2015

    • Search Google Scholar
    • Export Citation
  • 7

    Coenen VA, Honey CR, Hurwitz T, Rahman AA, McMaster J, Bürgel U, : Medial forebrain bundle stimulation as a pathophysiological mechanism for hypomania in subthalamic nucleus deep brain stimulation for Parkinson’s disease. Neurosurgery 64:11061115, 2009

    • Search Google Scholar
    • Export Citation
  • 8

    Coenen VA, Panksepp J, Hurwitz TA, Urbach H, Mädler B: Human medial forebrain bundle (MFB) and anterior thalamic radiation (ATR): imaging of two major subcortical pathways and the dynamic balance of opposite affects in understanding depression. J Neuropsychiatry Clin Neurosci 24:223236, 2012

    • Search Google Scholar
    • Export Citation
  • 9

    Coenen VA, Schlaepfer TE, Maedler B, Panksepp J: Cross-species affective functions of the medial forebrain bundle—implications for the treatment of affective pain and depression in humans. Neurosci Biobehav Rev 35:19711981, 2011

    • Search Google Scholar
    • Export Citation
  • 10

    Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N: Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482:8588, 2012

    • Search Google Scholar
    • Export Citation
  • 11

    Cordella R, Carella F, Franzini A, Marras C, Villani F, Messina G, : Intraoperative microrecordings in the posterior hypothalamus of anaesthetized humans with aggressive behaviour. Neurol Sci 31:183188, 2010

    • Search Google Scholar
    • Export Citation
  • 12

    Döbrössy MD, Furlanetti LL, Coenen VA: Electrical stimulation of the medial forebrain bundle in pre-clinical studies of psychiatric disorders. Neurosci Biobehav Rev 49:3242, 2015

    • Search Google Scholar
    • Export Citation
  • 13

    Espinoza J, Escobar O, Benedetti J: Functional neurosurgery for impulsive aggression: long term follow up. Stereotact Funct Neurosurg 90 (Suppl 1):94, 2012 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 14

    Franzini A, Marras C, Ferroli P, Bugiani O, Broggi G: Stimulation of the posterior hypothalamus for medically intractable impulsive and violent behavior. Stereotact Funct Neurosurg 83:6366, 2005

    • Search Google Scholar
    • Export Citation
  • 15

    Hall RCW: Global assessment of functioning. A modified scale. Psychosomatics 36:267275, 1995

  • 16

    Hernando V, Pastor J, Pedrosa M, Peña E, Sola RG: Low-frequency bilateral hypothalamic stimulation for treatment of drug-resistant aggressiveness in a young man with mental retardation. Stereotact Funct Neurosurg 86:219223, 2008

    • Search Google Scholar
    • Export Citation
  • 17

    Jiménez F, Soto JE, Velasco F, Andrade P, Bustamante JJ, Gómez P, : Bilateral cingulotomy and anterior capsulotomy applied to patients with aggressiveness. Stereotact Funct Neurosurg 90:151160, 2012

    • Search Google Scholar
    • Export Citation
  • 18

    Jiménez F, Soto JE, Velasco F, Andrade P, Bustamante JJ, Gómez P, : Long-term results of posteromedial hypothalamic deep brain stimulation in resistant epilepsy associated to aggressive behavior. Stereotact Funct Neurosurg 92 (Suppl 2):s106, 2014 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 19

    Kuhn J, Lenartz D, Mai JK, Huff W, Klosterkoetter J, Sturm V: Disappearance of self-aggressive behaviour in a brain-injuried patient after deep brain stimulation of the hypothalamus: technical case report. Neurosurgery 62:E1182, 2008

    • Search Google Scholar
    • Export Citation
  • 20

    Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, : Input-specific control of reward and aversion in the ventral tegmental area. Nature 491:212217, 2012

    • Search Google Scholar
    • Export Citation
  • 21

    Mayanagi Y, Hori T, San K: The posteromedial hypothalamus and pain, behavior, with special reference to endocrinological findings. Appl Neurophysiol 41:223231, 1978

    • Search Google Scholar
    • Export Citation
  • 22

    Meola A, Yeh FC, Fellows-Mayle W, Weed J, Fernandez-Miranda JC: Human connectome-based tractographic atlas of the brainstem connections and surgical approaches. Neurosurgery 79:437455, 2016

    • Search Google Scholar
    • Export Citation
  • 23

    Micieli R, Rios ALL, Aguilar RP, Posada LFB, Hutchison WD: Single-unit analysis of the human posterior hypothalamus and red nucleus during deep brain stimulation for aggressivity. J Neurosurg 126:11581164, 2017

    • Search Google Scholar
    • Export Citation
  • 24

    Miller S, Akram H, Lagrata S, Hariz M, Matharu M, Zrinzo L: EHMTI-0279. Deep brain stimulation for refractory chronic cluster headache. J Headache Pain 15 (Suppl 1):C44, 2014 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 25

    Morales M, Margolis EB: Ventral tegmental area: cellular heterogeneity, connectivity and behaviour. Nat Rev Neurosci 18:7385, 2017

  • 26

    Naftolowitz DF, Donovan S, Frances A: DSM-IV. Implications for drug therapy. CNS Drugs 4:17, 1995

  • 27

    Narabayashi H, Nagao T, Saito Y, Yoshida M, Nagahata M: Stereotaxic amygdalotomy for behavior disorders. Arch Neurol 9:116, 1963

  • 28

    Owen SLF, Green AL, Davies P, Stein JF, Aziz TZ, Behrens T, : Connectivity of an effective hypothalamic surgical target for cluster headache. J Clin Neurosci 14:955960, 2007

    • Search Google Scholar
    • Export Citation
  • 29

    Parent AD, Perkins E: The hypothalamus, in Haines DE, Mihailoff GA (eds): Fundamental Neuroscience for Basic and Clinical Applications, ed 5. Philadelphia: Elsevier, 2017

    • Search Google Scholar
    • Export Citation
  • 30

    Ramamurthi B: Stereotactic operation in behaviour disorders. Amygdalotomy and hypothalamotomy. Acta Neurochir Suppl (Wien) 44:152157, 1988

    • Search Google Scholar
    • Export Citation
  • 31

    Rizzi M, Trezza A, Messina G, De Benedictis A, Franzini A, Marras CE: Exploring the brain through posterior hypothalamus surgery for aggressive behavior. Neurosurg Focus 43(3):E14, 2017

    • Search Google Scholar
    • Export Citation
  • 32

    Rosa M, Franzini A, Giannicola G, Messina G, Altamura AC, Priori A: Hypothalamic oscillations in human pathological aggressiveness. Biol Psychiatry 72:e33e35, 2012

    • Search Google Scholar
    • Export Citation
  • 33

    Sano K, Mayanagi Y: Posteromedial hypothalamotomy in the treatment of violent, aggressive behavior. Act Neurochir Suppl (Wien) 44:145151, 1988

    • Search Google Scholar
    • Export Citation
  • 34

    Sano K, Yoshioka M, Ogashiwa M, Ishijima B, Ohye C: Postero-medial hypothalamotomy in the treatment of aggressive behaviors. Confin Neurol 27:164167, 1966

    • Search Google Scholar
    • Export Citation
  • 35

    Schlaepfer TE, Bewernick BH, Kayser S, Mädler B, Coenen VA: Rapid effects of deep brain stimulation for treatment-resistant major depression. Biol Psychiatry 73:12041212, 2013

    • Search Google Scholar
    • Export Citation
  • 36

    Schvarcz JR, Driollet R, Rios E, Betti O: Stereotactic hypothalamotomy for behaviour disorders. J Neurol Neurosurg Psychiatry 35:356359, 1972

    • Search Google Scholar
    • Export Citation
  • 37

    Sramka M, Pogády P, Csoková Z, Pogády J: [Long-term results in patients with stereotaxic surgery for psychopathologic disorders.] Bratisl Lek Listy 93:364366, 1992 (Slovak)

    • Search Google Scholar
    • Export Citation
  • 38

    Torres CV, Ezquiaga E, Navas M, García Pallero MA, Sola RG: Long-term results of deep brain stimulation of the subcallosal cingulate for medication-resistant bipolar I depression and rapid cycling bipolar II depression. Biol Psychiatry 81:e33e34, 2017

    • Search Google Scholar
    • Export Citation
  • 39

    Torres CV, Manzanares R, Sola RG: Integrating diffusion tensor imaging-based tractography into deep brain stimulation surgery: a review of the literature. Stereotact Funct Neurosurg 92:282290, 2014

    • Search Google Scholar
    • Export Citation
  • 40

    Torres CV, Sola RG, Pastor J, Pedrosa M, Navas M, García-Navarrete E, : Aggressive behavior. response. J Neurosurg 120:287288, 2014

  • 41

    Torres CV, Sola RG, Pastor J, Pedrosa M, Navas M, García-Navarrete E, : Long-term results of posteromedial hypothalamic deep brain stimulation for patients with resistant aggressiveness. J Neurosurg 119:277287, 2013

    • Search Google Scholar
    • Export Citation
  • 42

    Wada T, Kayaba T: Dorsomedial thalamotomy (V). Results of psychological examination. Tohoku J Exp Med 54:247249, 1951

  • 43

    Weatherman R, Bruininks RH, Hill B, Woodcock R: Inventory for client and agency planning. Rural Spec Educ Q 6:5859, 1986

Metrics

All Time Past Year Past 30 Days
Abstract Views 1205 752 39
Full Text Views 184 80 5
PDF Downloads 103 56 5
EPUB Downloads 0 0 0