Research

Themes

I. Mechanisms of action of neuromodulation therapies: deep brain stimulation (DBS) and focused ultrasound (FUS) 

II. Clinical trials of surgery for movement, pain and psychiatric disorders

III. Neural prostheses

IV. Physiology of the human basal ganglia and thalamus 

V. Neuroethics in neuromodulation 
 

I. Mechanisms of action of neuromodulation therapies

[neuron03scale.tif + patched-cell.jpg]

Our research aims are to understand how neuromodulation therapies work. DBS electrodes are placed in various deep brain nuclei for the treatment of movement disorders (essential tremor, Parkinson’s disease, dystonia), pain, epilepsy, depression, and obsessive-compulsive disorder. The clinical benefits of DBS are well recognized; however, its mechanism of action is less so. Our lab has developed a good understanding of mechanisms of thalamic DBS for tremor (Neurosci 2002, J Physiol 2004, J Neurosci 2006, J Neurophysiol 2006), others have dissected how subthalamic STN DBS works. While we have made inroads (PlosOne 2014, J Neurophysiol 2016, J Neurosci 2018), how DBS works for dystonia remains an open question. And mechanisms of benefit for depression are even more puzzling (Eur Neuropsychopharmacol 2021).

Focused ultrasound (FUS) is the newest treatment technique and at high intensity it can lesion brain targets. However at lower intensities and by applying different patterns, it may modulate neural tissue thereby non-invasively and focally altering neural function. How FUS neuromodulation works is also unknown.

Using a combined approach of direct examination of beneficial effects of DBS and FUS in patients, intra-operative microelectrode recording/stimulation, applying FUS / DBS to brain slices, and in behaving animal models, we hope to understand its mode of action. With a better understanding of how both these therapies work, we can optimize its application and apply them to novel brain nuclei to treat new conditions.
 

II. Clinical trials of surgery for movement, pain and psychiatric disorders

While DBS and FUS seems to help several neurological and psychiatric conditions, in order to prove benefit well-designed and controlled clinical studies are essential. Our group was the first to perform a multicentre clinical trial for DBS in Canada (Brain 2007). We have previously led a multicentre randomized controlled double-blind trial of hippocampal DBS for epilepsy, participated in a multicentre cross-over trial of motor cortex stimulation for neuropathic pain (Can J Neurol Sci 2015), and an industry-sponsored trial of occipital nerve region stimulation for migraine (Cephalalgia 2011). We performed a randomized trial of different DBS parameters for treatment-resistant depression (Lancet Psychiatry 2020), identifying several biomarkers of response (J Affective Disord 2020, Neuropsychopharmacology 2020, Brain Stim 2020 and 2022). 
 

III. Smart neural prostheses to restore lost function

Smart prosthetics are in their infancy, but they are one of the newest fields of neuroscience. While there are many challenges faced in this arena we have focused on sensory restoration of touch and kinesthesis (J Neural Eng 2010 and 2018, Trans Neural Syst Rehabil Eng 2011). We continue to test various stimulation methods and ways to improve naturalness of electrical stimulation-induced percepts in patients undergoing surgery.
 

IV. Human systems physiology and disease pathophysiologyWhile smart prosthetics are exciting and novel, we still do not understand how the nervous system works well enough to interact with it in a meaningful manner. 

We have been recording single and multiple neuronal firing in the human thalamus, pallidum, striatum, subthalamic regions and other subcortical regions with microelectrodes for more than two decades, as part of routine surgery to determine the optimal spot for DBS electrode placement. This provides a unique opportunity to study the firing rates, patterns and receptive fields of the neurons we encounter, thereby helping us understand the function of these nuclei and the sensorimotor system as a whole. We have identified electrophysiological markers of disease in depression (Biol Psychiatry 2016), dystonia (J Neurol Neurosurg Psychiatry 2014) and continue to explore the pathophysiology of PD and dystonia using multimodal imaging and electrophysiology. 

V. Ethics in neuromodulation
Collaborative work with the UBC Centre for Neuroethics has reported on patents in neuromodulation therapies (Nature Biotechnol 2017, Neuromodulation 2019). We continue to examine the patent landscape and the flow of funding for neuromodulation intellectual property (IP).   

 

PUBLICATIONS

CURRICULUM VITAE 

Zelma Kiss, MD PhD FRCSC 
Professor, Department of Clinical Neurosciences
Hotchkiss Brain Institute, University of Calgary
 

SELECTED PUBLICATIONS (* next to our lab trainees) 

Swytink-Binnema CA*, Rockel CP, Martino D, Dukelow SP, Pike GB, Kiss ZHT: Limb preference changes after focused-ultrasound thalamotomy for tremor. Mov Disord. 38(5):831-842, 2023. [PMID: 36947685]
 

An S, Fousek J, Kiss ZHT, Cortese F, van der Wijk G, McAusland LB, Ramasubbu R, Jirsa VK, Protzner AB: High-resolution Virtual Brain modeling personalizes deep brain stimulation for treatment-resistant depression: Spatiotemporal response characteristics following stimulation of neural fibre pathways. Neuroimage. 249:118848249:118848, 2022.  [PMID: 34954330]
 

Luo F*, Kiss ZHT: Cholinergics contribute to the cellular mechanisms of deep brain stimulation applied in rat infralimbic cortex but not white matter. Eur. Neuropsychopharmacol 45:52-58 2021. [PMID: 33771420]
 

Ramasubbu R, Clark DL*, Golding S, Dobson KS, Mackie A, Haffenden A, Kiss ZHT: Long versus short pulse width subcallosal cingulate stimulation for treatment-resistant depression: A randomised, double-blind, crossover trial. Lancet Psychiatry 7(1): 29-40, 2020. [PMID: 31860455]
 

Martino D, Rockel C, Bruno V, Mazerolle EL, Jetha S, Pichardo S, Pike GB, Kiss ZHT: Dystonia following thalamic neurosurgery: A single centre experience with MR-guided focused ultrasound thalamotomy. Parkinsonism Relat Disord. 71:1-3, 2020. [PMID: 31923520]
 

Clark DL*, MacMaster FP, Brown EC*, Kiss ZHT, Ramasubbu R: Anterior cingulate glutamate predicts response to subcallosal cingulate deep brain stimulation for treatment-resistant depression. J Affective Disord 266: 92-94, 2020. [PMID: 32056951]
 

Noor MS*, Yu L, Murari K, Kiss ZHT: Neurovascular coupling during deep brain stimulation. Brain Stimul 13(3): 916-927, 2020. [PMID: 32289725]
 

Clark DL*, Johnson K, Butson C, Lebel C, Gobbi D, Ramasubbu R, Kiss ZHT: Tract-based analysis of target engagement by subcallosal cingulate DBS for treatment resistant depression. Brain Stimul 13(4): 1094-1101, 2020. [PMID: 32417668]
 

Brown EC*, Clark DL*, Forkert ND, Molnar CP, Kiss ZHT, Ramasubbu R: Metabolic activity in subcallosal cingulate predicts response to deep brain stimulation for depression. Neuropsychopharmacology 45(10):1681-1688, 2020. [PMID: 32580207]
 

Luo F*, Kim LH*, Magown P, Noor MS*, Kiss ZHT: Long-lasting electrophysiological after-effects of high frequency stimulation in the globus pallidus: human and rodent slice studies. J Neurosci 38(50): 10734-10746, 2018. [PMID: 30373767]
 

Kim LH*, McLeod RS, Kiss ZHT: A new psychometric questionnaire for reporting of somatosensory percepts. J Neural Eng 15(1):013002, 2018. [PMID: 29076455]
 

Roskams-Edris D, Anderson-Redick S, Kiss ZHT*, Illes J* (*co-corresponding authors): Situating brain regions among patent rights and ethical wrongs. Nat Biotechnol 35(2): 119-121, 2017. [PMID: 28178252] 
 

Noor MS*, Murari K, McCracken CB*, Kiss ZHT: Spatiotemporal dynamics of cortical perfusion in response to thalamic deep brain stimulation. Neuroimage 126: 131-139, 2016. [PMID: 26578359] {*our figure was selected as the cover image for this volume}
 

Clark DL*, Brown EC*, Ramasubbu R, Kiss ZHT: Intrinsic beta oscillations in the subgenual cingulate relate to symptoms in treatment resistant depression. Biol Psychiatry pii: S0006-3223(16)31113-1, 2016. [PMID: 27129412]
 

Lee JR*, Kiss ZHT: Interhemispheric difference of pallidal local field potential activity in cervical dystonia. J Neurol Neurosurg Psychiatry. 85:306-310, 2014. [PMID: 23990682]
 

Wile DJ, Ranawaya R, Kiss ZHT: Smart watch accelerometry for analysis and diagnosis of tremor. J Neurosci Methods. 230: 1-4, 2014. [PMID: 24769376]
 

McCracken CB*, Kiss ZHT: Time- and frequency-dependent modulation of local field potential synchronization by deep brain stimulation. PLoS One 9(7): e102576, 2014. [PMID: 25029468]
 

Denheyer M, Kiss ZHT, Haffenden AM: Behavioral effects of subthalamic deep brain stimulation in Parkinson’s disease. Neuropsychologia 47(14): 3203-9, 2009. [PMID: 19664645]
 

Kiss ZHT, Doig-Beyaert K, Eliasziw M, Tsui J, Haffenden AM, Suchowersky O, for the Canadian Neurosurgical Society Stereotactic/Functional Section and the Canadian Movement Disorders Group. The Canadian multicentre study of deep brain stimulation for cervical dystonia. Brain 130 (Pt 11):2879-2886, 2007. [PMID: 17905796]
 

Anderson TR*, Hu B, Iremonger KJ, Kiss ZHT: Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation induced tremor arrest. J Neurosci 26(3): 841-850, 2006. [PMID: 15218068]
 

Iremonger KJ*, Anderson TR*, Hu B, Kiss ZHT: Cellular mechanisms preventing sustained activation of cortex during subcortical high frequency stimulation. J Neurophysiol 96(2): 613-621, 2006. [PMID: 16554516]
 

Anderson TR*, Hu B, Pittman Q, Kiss ZHT: Mechanisms of deep brain stimulation: An intracellular study in rat thalamus. J Physiol 559(Pt 1):301-313, 2004. [PMID: 15218068]
 

Kiss ZHT, Mooney DM, Renaud LP, Hu B: Neuronal response to local electrical stimulation in rat thalamus: Physiological implications for mechanisms of deep brain stimulation. Neuroscience 113(1):137-143, 2002.  [PMID: 15264774]
 

Davis KD, Kiss ZHT, Luo L*, Tasker RR, Lozano AM, Dostrovsky JO: Phantom sensations generated by thalamic microstimulation. Nature 391:385-387, 1998. [PMID: 9450753]
 

Lozano AM, Hutchison WD, Kiss ZHT, Tasker RR, Davis KD, Dostrovsky JO: Methods for microelectrode-guided posteroventral pallidotomy. J Neurosurg 84:194-202, 1996.  [PMID: 8592221]
 

ONGOING FUNDING
 

2018-2023: Canada Foundation for Innovation 

MR Guided Focused Ultrasound Research Platform

PI: GB Pike; Co-Applicants: G Cairncross, J Dunn, R Frayne, A Kirton, Z Kiss, D. Martino, O Monchi, G Sutherland, P Whelan

 

2021-2024:  ERA-NET (Research Projects on Ethical, Legal and Social Aspects of Neuroscience) NEURON (Network for European Funding for Neuroscience Research)

Canadian Institutes of Health Research contribution 

International Neuroethics Patent Initiative

PIs: Spranger (Germany) and Illes (Canada); co-PI (Canada): Kiss

 

2022-2024: HBI/DCNS Pilot Research Fund Program 

Title: Developing a new LIFU neuromodulation method to suppress tremor
 

2022-2025: CaPRI -HBI Movement disorders Neuroteam pilot project 

Title: Electrophysiological markers of long-term benefit vs. early cognitive decline in PD patients treated with STN-DBS
 

2023-2024: Parkinson Canada Pilot Project Grant 

Restoration of locomotor function following stimulation of the A13 region in Parkinson’s rat models.

PI: Whelan; co-I: Kiss, Murari, Park

 

2023-2028: Natural Sciences and Engineering Research Council of Canada (NSERC) 

Discovery Grant Renewal: Mechanisms of low intensity focused ultrasound neural modulation