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Acta Neurochirurgica

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01-08-2014 | Technical Note - Functional

A step-wise approach to deep brain stimulation in mice

Authors: Casey H. Halpern, Mark A. Attiah, Anand Tekriwal, Gordon H. Baltuch

Published in: Acta Neurochirurgica | Issue 8/2014

Abstract

Background

Studies of deep brain stimulation (DBS) in mice are rare due to their small size, agility, aversion to handling, and high anxiety compared to larger species. Studying DBS modulation of neural circuitry in murine models of human behavior may ensure safety, guide stimulatory parameters for clinical trials in humans, and inform a long-eluded mechanism.

Methods

Stereotactic deep brain electrode implantation in a mouse is performed. Mechanical etching of the skull with a high-speed drill is used with placement of cyanoacrylate glue and molding of dental acrylate to affix the electrode in place. Stimulation experiments are conducted in the home cage after a habituation period. After testing is complete, electrode placement is verified in fixed tissue.

Results

Electrodes can be safely and accurately implanted in mice for DBS experimentation. Previous findings demonstrated accuracy in placement within the nucleus accumbens shell of 93 % [14]. In this study, there were no hardware malfunctions that required interrupting experimentation.

Conclusions

Stereotactic DBS studies may be safely and effectively performed in mice to investigate neuropsychiatric disorders. In addition, examining the biochemical and molecular mechanisms underlying these disorders may be facilitated by widely available transgenic mouse lines and the Cre-Lox recombination system.

Agterberg MJH, Spoelstra EN, Van Der Wijst S, Brakkee JH, Wiegant VM, Hamelink R, Brouns K, Westerink BH, Remie R (2010) Evaluation of temperature rise and bonding strength in cements used for permanent head attachments in rats and mice. Lab Anim 44(3):264–270PubMedCrossRef

Albertin SV, Mulder AB, Tabuchi E, Zugaro MB, Wiener SI (2000) Lesions of the medial shell of the nucleus accumbens impair rats in finding larger rewards, but spare reward-seeking behavior. Behav Brain Res 117(1–2):173–183PubMedCrossRef

Benabid AL, Pollak P, Louveau A, Henry S, de Rougemont J (1987) Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol 50(1–6):344–346PubMed

Benazzouz A, Hallett M (2000) Mechanism of action of deep brain stimulation. Neurology 55(12 Suppl 6):S13–S16PubMed

Benazzouz A, Gross C, Féger J, Boraud T, Bioulac B (1993) Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur J Neurosci 5(4):382–389PubMedCrossRef

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(9):1975–1985PubMedCentralPubMedCrossRef

Breit S, Schulz JB, Benabid A-L (2004) Deep brain stimulation. Cell Tissue Res 318(1):275–288PubMedCrossRef

Chang J-Y, Shi L-H, Luo F, Woodward DJ (2003) High-frequency stimulation of the subthalamic nucleus improves treadmill locomotion in unilateral 6-hydroxydopamine lesioned rats. Brain Res 983(1–2):174–184PubMedCrossRef

Chuhma N, Tanaka KF, Hen R, Rayport S (2011) Functional connectome of the striatal medium spiny neuron. J Neurosci 31(4):1183–1192PubMedCentralPubMedCrossRef

10.

David SP, Munafò MR, Johansen-Berg H, Smith SM, Rogers RD, Matthews PM, Walton RT (2005) Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: a functional magnetic resonance imaging study. Biol Psychiatry 58(6):488–494PubMedCrossRef

11.

Dostrovsky JO, Levy R, Wu JP, Hutchison WD, Tasker RR, Lozano AM (2000) Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J Neurophysiol 84(1):570–574PubMed

12.

Dostrovsky JO, Lozano AM (2002) Mechanisms of deep brain stimulation. Mov Disord 17(Suppl 3):S63–S68PubMedCrossRef

13.

Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324(5925):354–359PubMedCrossRef

14.

Halpern CH, Tekriwal A, Santollo J, Keating JG, Wolf JA, Daniels D, Bale TL (2013) Amelioration of binge eating by nucleus accumbens shell deep brain stimulation in mice involves d2 receptor modulation. J Neurosci 33(17):7122–7129PubMedCentralPubMedCrossRef

15.

Halpern C, Hurtig H, Jaggi J, Grossman M, Won M, Baltuch G (2007) Deep brain stimulation in neurologic disorders. Parkinsonism Relat Disord 13(1):1–16PubMedCrossRef

16.

Hamani C, Diwan M, Macedo CE, Brandão ML, Shumake J, Gonzalez-Lima F, Raymond R, Lozano AM, Fletcher PJ, Nóbrega JN (2010) Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats. Biol Psychiatry 67(2):117–124PubMedCrossRef

17.

Hamani C, Machado DC, Hipólide DC, Dubiela FP, Suchecki D, Macedo CE, Tescarollo F, Martins U, Covolan L, Nóbrega JN (2012) Deep brain stimulation reverses anhedonic-like behavior in a chronic model of depression: role of serotonin and brain derived neurotrophic factor. Biol Psychiatry 71(1):30–35PubMedCrossRef

18.

Kelley AE, Baldo BA, Pratt WE, Will MJ (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86(5):773–795PubMedCrossRef

19.

Lobo MK, Covington HE, Chaudhury D, Friedman AK, Sun H, Damez-Werno D, Dietz DM, Zaman S, Koo JW, Kennedy PJ, Mouzon E, Mogri M, Neve RL, Deisseroth K, Han MH, Nestler EJ (2010) Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330(6002):385–390PubMedCentralPubMedCrossRef

20.

Longordo F, Fan J, Steimer T, Kopp C, Lüthi A (2011) Do mice habituate to “gentle handling?” A comparison of resting behavior, corticosterone levels and synaptic function in handled and undisturbed C57BL/6 J mice. Sleep 34(5):679–681PubMedCentralPubMed

21.

Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, Schwalb JM, Kennedy SH (2005) Deep brain stimulation for treatment-resistant depression. Neuron 45(5):651–660PubMedCrossRef

22.

Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15(24):2279–2284PubMedCrossRef

23.

Nutt JG, Rufener SL, Carter JH, Anderson VC, Pahwa R, Hammerstad JP, Burchiel KJ (2001) Interactions between deep brain stimulation and levodopa in Parkinson’s disease. Neurology 57(10):1835–1842PubMedCrossRef

24.

O’Suilleabhain PE, Frawley W, Giller C, Dewey RB (2003) Tremor response to polarity, voltage, pulsewidth and frequency of thalamic stimulation. Neurology 60(5):786–790PubMedCrossRef

25.

Okun MS, Green J, Saben R, Gross R, Foote KD, Vitek JL (2003) Mood changes with deep brain stimulation of STN and GPi: results of a pilot study. J Neurol Neurosurg Psychiatr 74(11):1584–1586PubMedCentralPubMedCrossRef

26.

Paxinos G, Franklin KBJ (2004) The mouse brain in stereotaxic coordinates. Academic Press, Waltham

27.

Pizzagalli DA, Holmes AJ, Dillon DG, Goetz EL, Birk JL, Bogdan R, Dougherty DD, Iosifescu DV, Rauch SL, Fava M (2009) Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. Am J Psychiatry 166(6):702–710PubMedCentralPubMedCrossRef

28.

Rothwell PE, Kourrich S, Thomas MJ (2011) Environmental novelty causes stress-like adaptations at nucleus accumbens synapses: implications for studying addiction-related plasticity. Neuropharmacology 61(7):1152–1159PubMedCentralPubMedCrossRef

29.

Salin P, Manrique C, Forni C, Kerkerian-Le Goff L (2002) High-frequency stimulation of the subthalamic nucleus selectively reverses dopamine denervation-induced cellular defects in the output structures of the basal ganglia in the rat. J Neurosci 22(12):5137–5148PubMed

30.

Schlaepfer T, Cohen M, Frick C, Kosel M, Brodesser D, Axmacher N, Joe A, Kreft M, Lenartz D, Sturm V (2007) Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33(2):368–377PubMedCrossRef

31.

Shon Y-M, Lee KH, Goerss SJ, Kim IY, Kimble C, Gompel JJV, Bennet K, Blaha CD, Chang S-Y (2010) High-frequency stimulation of the subthalamic nucleus evokes striatal dopamine release in a large animal model of human DBS neurosurgery. Neurosci Lett 475(3):136–140PubMedCentralPubMedCrossRef

32.

Sturm V, Lenartz D, Koulousakis A, Treuer H, Herholz K, Klein JC, Klosterkötter J (2003) The nucleus accumbens: a target for deep brain stimulation in obsessive–compulsive- and anxiety-disorders. J Chem Neuroanat 26(4):293–299PubMedCrossRef

33.

Szczesny G, Veihelmann A, Massberg S, Nolte D, Messmer K (2004) Long-term anaesthesia using inhalatory isoflurane in different strains of mice-the haemodynamic effects. Lab Anim 38(1):64–69PubMedCrossRef

34.

Tsai H-C, Zhang F, Adamantidis A, Stuber GD, Bonci A, de Lecea L, Deisseroth K (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324(5930):1080–1084PubMedCrossRef

35.

Vassoler FM, Schmidt HD, Gerard ME, Famous KR, Ciraulo DA, Kornetsky C, Knapp CM, Pierce RC (2008) Deep brain stimulation of the nucleus accumbens shell attenuates cocaine priming-induced reinstatement of drug seeking in rats. J Neurosci 28(35):8735–8739PubMedCentralPubMedCrossRef

36.

Vitek JL (2002) Mechanisms of deep brain stimulation: excitation or inhibition. Mov Disord 17(Suppl 3):S69–S72PubMedCrossRef

37.

Windels F, Bruet N, Poupard A, Feuerstein C, Bertrand A, Savasta M (2003) Influence of the frequency parameter on extracellular glutamate and gamma-aminobutyric acid in substantia nigra and globus pallidus during electrical stimulation of subthalamic nucleus in rats. J Neurosci Res 72(2):259–267PubMedCrossRef

38.

Witten IB, Lin S-C, Brodsky M, Prakash R, Diester I, Anikeeva P, Gradinaru V, Ramakrishnan C, Deisseroth K (2010) Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330(6011):1677–1681PubMedCentralPubMedCrossRef

39.

Wu C, Wais M, Zahid T, Wan Q, Zhang L (2009) An improved screw-free method for electrode implantation and intracranial electroencephalographic recordings in mice. Behav Res Methods 41(3):736–741PubMedCrossRef

Title: A step-wise approach to deep brain stimulation in mice
Authors: Casey H. Halpern
Mark A. Attiah
Anand Tekriwal
Gordon H. Baltuch
Publication date: 01-08-2014
Publisher: Springer Vienna
Published in: Acta Neurochirurgica / Issue 8/2014
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-014-2062-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

A step-wise approach to deep brain stimulation in mice

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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