Temporal pattern of electrical stimulation is a new dimension of therapeutic innovation

Grill, Warren M.

doi:10.1016/j.cobme.2018.08.007

Cited by 52 publications

(41 citation statements)

References 54 publications

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“…Neuronal representation of sensory information is highly complex (Lieber & Bensmaia, 2019), and the ability to selectively recruit neuronal populations proximal to the electrode by varying pulse amplitude, frequency, or polarity could provide the ability to stimulate neural activity that matches physiological response patterns (Anderson, Duffley, Vorwerk, Dorval, & Butson, 2018; Cai et al., 2017; Delhaye, Saal, & Bensmaia, 2016; Grill, 2018; Histed, Bonin, & Reid, 2009; Hofmann, Ebert, Tass, & Hauptmann, 2011; Koivuniemi & Otto, 2011; Kuncel & Grill, 2004; Macherey, van Wieringen, Carlyon, Deeks, & Wouters, 2006; McIntyre & Grill, 2000, 2002; McIntyre, Richardson, & Grill, 2002; Michelson, Eles, Vazquez, Ludwig, & Kozai, 2019). For example, neuronal adaptation is a common response to sustained stimuli and is believed to allow the brain to better respond to transient stimuli (Wark, Lundstrom, & Fairhall, 2007).…”

Section: Introductionmentioning

confidence: 99%

In vivo microstimulation with cathodic and anodic asymmetric waveforms modulates spatiotemporal calcium dynamics in cortical neuropil and pyramidal neurons of male mice

Stieger

Eles

Ludwig

et al. 2020

J of Neuroscience Research

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Electrical stimulation has been critical in the development of an understanding of brain function and disease. Despite its widespread use and obvious clinical potential, the mechanisms governing stimulation in the cortex remain largely unexplored in the context of pulse parameters. Modeling studies have suggested that modulation of stimulation pulse waveform may be able to control the probability of neuronal activation to selectively stimulate either cell bodies or passing fibers depending on the leading polarity. Thus, asymmetric waveforms with equal charge per phase (i.e., increasing the leading phase duration and proportionately decreasing the amplitude) may be able to activate a more spatially localized or distributed population of neurons if the leading phase is cathodic or anodic, respectively. Here, we use two‐photon and mesoscale calcium imaging of GCaMP6s expressed in excitatory pyramidal neurons of male mice to investigate the role of pulse polarity and waveform asymmetry on the spatiotemporal properties of direct neuronal activation with 10‐Hz electrical stimulation. We demonstrate that increasing cathodic asymmetry effectively reduces neuronal activation and results in a more spatially localized subpopulation of activated neurons without sacrificing the density of activated neurons around the electrode. Conversely, increasing anodic asymmetry increases the spatial spread of activation and highly resembles spatiotemporal calcium activity induced by conventional symmetric cathodic stimulation. These results suggest that stimulation polarity and asymmetry can be used to modulate the spatiotemporal dynamics of neuronal activity thus increasing the effective parameter space of electrical stimulation to restore sensation and study circuit dynamics.

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Section: Introductionmentioning

confidence: 99%

In vivo microstimulation with cathodic and anodic asymmetric waveforms modulates spatiotemporal calcium dynamics in cortical neuropil and pyramidal neurons of male mice

Stieger

Eles

Ludwig

et al. 2020

J of Neuroscience Research

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“…This stands in contrast to the mean spike rate or periodicity code that are often proposed to be neural codes for frequency perception in higher neural centres [6][7][8][9]. Electrical burst stimulation has been suggested to be useful in restoring the sense of touch in amputees using a prosthesis [10][11][12] or in the treatment of movement disorders through deep brain stimulation [13][14][15]. These studies were generally concerned with the efficacy of inducing neural activity, rather than the effect of burst stimulation on information encoding.…”

Section: Introductionmentioning

confidence: 99%

Temporal patterns in electrical nerve stimulation: Burst gap code shapes tactile frequency perception

Olausson

Vickery

et al. 2020

PLoS ONE

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We have previously described a novel temporal encoding mechanism in the somatosensory system, where mechanical pulses grouped into periodic bursts create a perceived tactile frequency based on the duration of the silent gap between bursts, rather than the mean rate or the periodicity. This coding strategy may offer new opportunities for transmitting information to the brain using various sensory neural prostheses and haptic interfaces. However, it was not known whether the same coding mechanisms apply when using electrical stimulation, which recruits a different spectrum of afferents. Here, we demonstrate that the predictions of the burst gap coding model for frequency perception apply to burst stimuli delivered with electrical pulses, re-emphasising the importance of the temporal structure of spike patterns in neural processing and perception of tactile stimuli. Reciprocally, the electrical stimulation data confirm that the results observed with mechanical stimulation do indeed depend on neural processing mechanisms in the central nervous system, and are not due to skin mechanical factors and resulting patterns of afferent activation.

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“…The application of other biomarkers or multiple biomarkers in the design of closed-loop stimulation for PD is worth exploring (Hoang et al, 2017). The controller regulated the stimulation frequency, but the effects of DBS are also dependent on the pulse amplitude, pulse duration, and stimulation pattern (Kuncel and Grill, 2004; Grill, 2018). Further, Holt et al demonstrated that the effects of burst DBS in a network model of the basal ganglia (Hahn and McIntyre, 2010) were strongly dependent on timing relative to the phase of oscillatory activity (Holt et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Model-Based Evaluation of Closed-Loop Deep Brain Stimulation Controller to Adapt to Dynamic Changes in Reference Signal

Kumaravelu

Wang

et al. 2019

Front. Neurosci.

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High-frequency deep brain stimulation (DBS) of the subthalamic nucleus (STN) is effective in suppressing the motor symptoms of Parkinson's disease (PD). Current clinically-deployed DBS technology operates in an open-loop fashion, i.e., fixed parameter high-frequency stimulation is delivered continuously, invariant to the needs or status of the patient. This poses two major challenges: (1) depletion of the stimulator battery due to the energy demands of continuous high-frequency stimulation, (2) high-frequency stimulation-induced side-effects. Closed-loop deep brain stimulation (CL DBS) may be effective in suppressing parkinsonian symptoms with stimulation parameters that require less energy and evoke fewer side effects than open loop DBS. However, the design of CL DBS comes with several challenges including the selection of an appropriate biomarker reflecting the symptoms of PD, setting a suitable reference signal, and implementing a controller to adapt to dynamic changes in the reference signal. Dynamic changes in beta oscillatory activity occur during the course of voluntary movement, and thus there may be a performance advantage to tracking such dynamic activity. We addressed these challenges by studying the performance of a closed-loop controller using a biophysically-based network model of the basal ganglia. The model-based evaluation consisted of two parts: (1) we implemented a Proportional-Integral (PI) controller to compute optimal DBS frequencies based on the magnitude of a dynamic reference signal, the oscillatory power in the beta band (13–35 Hz) recorded from model globus pallidus internus (GPi) neurons. (2) We coupled a linear auto-regressive model based mapping function with the Routh-Hurwitz stability analysis method to compute the parameters of the PI controller to track dynamic changes in the reference signal. The simulation results demonstrated successful tracking of both constant and dynamic beta oscillatory activity by the PI controller, and the PI controller followed dynamic changes in the reference signal, something that cannot be accomplished by constant open-loop DBS.

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Temporal pattern of electrical stimulation is a new dimension of therapeutic innovation

Cited by 52 publications

References 54 publications

In vivo microstimulation with cathodic and anodic asymmetric waveforms modulates spatiotemporal calcium dynamics in cortical neuropil and pyramidal neurons of male mice

In vivo microstimulation with cathodic and anodic asymmetric waveforms modulates spatiotemporal calcium dynamics in cortical neuropil and pyramidal neurons of male mice

Temporal patterns in electrical nerve stimulation: Burst gap code shapes tactile frequency perception

Model-Based Evaluation of Closed-Loop Deep Brain Stimulation Controller to Adapt to Dynamic Changes in Reference Signal

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