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Closed-Loop Neuromodulation in Physiological and Translational Research

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Closed-Loop Neuromodulation in Physiological and Translational Research Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Closed-Loop Neuromodulation in Physiological and Translational Research Stavros Zanos Translational Neurophysiology Laboratory, Center for Bioelectronic Medicine, Feinstein Institute for Medical Research, Northwell Health, Manhasset, New York 11030 Correspondence: [email protected] Neuromodulation, the focused delivery of energy to neural tissue to affect neural or physio- logical processes, is a common method to study the physiology of the nervous system. It is also successfully used as treatment for disorders in which the nervous system is affected or impli- cated. Typically, neurostimulation is delivered in open-loop mode (i.e., according to a pre- determined schedule and independently of the state of the organ or physiological system whose function is sought to be modulated). However, the physiology of the nervous system or the modulated organ can be dynamic, and the same stimulus may have different effects depending on the underlying state. As a result, open-loop stimulation may fail to restore the desired function or cause side effects. In such cases, a neuromodulation intervention may be preferable to be administered in closed-loop mode. In a closed-loop neuromodulation (CLN) system, stimulation is delivered when certain physiological states or conditions are met (responsive neurostimulation); the stimulation parameters can also be adjusted dynamically to optimize the effect of stimulation in real time (adaptive neurostimulation). In this review, the reasons and the conditions for using CLN are discussed, the basic components of a CLN system are described, and examples of CLN systems used in physiological and translational research are presented. ypically, in a physiology experiment, the sub- by the investigator and inferred by an automated Tject is exposed to a set of controlled condi- system that analyzes measurements taken si- tions and interventions, while the investigator multaneously, in real time (Fig. 1B). This exper- www.perspectivesinmedicine.org takes functional measurements. These measure- imental model can be useful in the study of the ments are recorded during the experiment to be nervous system owing to the inherently dynamic analyzed at a later time, offline (Fig. 1A). How- nature of neural activity because the same stim- ever, in some cases, the timing and other aspects ulus delivered against a different physiological of the intervention need to be linked to one or state may have completely different physiologi- more physiological events and physiological pa- cal effects. It can also be used as a method for rameters and tightly controlled, especially when controlling dynamic neural processes, as well those parameters change rapidly. In such cases, as other physiological functions that are them- the intervention is delivered on the occurrence selves modulated by the nervous system, in a of certain physiological states, defined a priori responsive and adaptive manner. In recent years, Editors: Valentin A. Pavlov and Kevin J. Tracey Additional Perspectives on Bioelectronic Medicine available at www.perspectivesinmedicine.org Copyright © 2018 Cold Spring Harbor Laboratory Press; all rights reserved Advanced Online Article. Cite this article as Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a034314 1 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press S. Zanos AB CPU Figure 1. Principles of open-loop and closed-loop experiments or interventions. (A) In an open-loop context, a predetermined intervention is applied to an animal according to a hypothesis, a set of measurements are taken to characterize the response of the animal to that intervention, and those measurements are analyzed at a later time by the investigator. (B) In a closed-loop context, the investigator starts by defining a set of rules that will determine the conditions at which an intervention will be applied to the animal. An automated system (CPU) observes a set of measurements taken from the animal at regular intervals and delivers the intervention according to the defined rules, in real time. the term neuromodulation has been adapted to studied, or when an intervention needs to hap- refer to these neural control systems, although in pen during a certain physiological state for it to the more traditional usage, neuromodulation is be successful. the physiological process by which a neuron uses In principle, the state dependency of the ef- chemicals to regulate the activity of large, often fects of neurostimulation on a dynamic neural or distant, populations of neurons. physiological process could be studied in either Here we will discuss the most common rea- of two ways in a given experiment: (1) open-loop sons for using a closed-loop neuromodulation delivery of stimuli across different physiological (CLN) approach and describe the basic compo- states and registration of physiological effects nents of closed-loop systems. Examples of CLN separately for each state, and (2) closed-loop de- systems in the context of basic and translational livery of stimuli in response to a specific state and physiological research will be presented. Finally, registration of the effects for that state only. In www.perspectivesinmedicine.org future directions of this line of research will be cases when the effects of neurostimulation are discussed. nonstationary and, more importantly, when they are affected by the history of neurostimula- tion itself, a closed-loop approach will more ac- REASONS AND CONDITIONS FOR THE USE curately address state-dependent effects. OF CLOSED-LOOP NEUROMODULATION One successful use of responsive CLN sys- There are two main reasons why one would tems in physiological research has been in in want to use a closed-loop approach in a neuro- vivo studies of synaptic plasticity. For spike modulation setting. timing-dependent synaptic potentiation to be induced, the detection of a spontaneous presyn- aptic action potential needs to be followed by Need for Responsive Neuromodulation electrical or sensory stimulation that elicits post- The requirement for responsive interaction with synaptic depolarization within a short window the nervous system arises when neural processes of time, typically, <50 msec (Dan and Poo 2004; that depend on precise timing between a phys- Jackson et al. 2006a; Nishimura et al. 2013a). iological event or state and an intervention are There are several examples of CLN systems 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a034314 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Closed-Loop Neuromodulation that, in real time, monitor neural or physiolog- number of preliminary human studies suggest ical activity, detect relevant signal signatures in it that closed-loop stimulation of the auricular (e.g., spikes, field potentials or muscle activity), branch of the vagus nerve (VN), triggered and deliver neurostimulation to successfully in- from the expiratory phase of the respiratory duce neural plasticity (Rebesco et al. 2010; Gug- rhythm, which is known to strongly modulate genmos et al. 2013; Ethier et al. 2015; Fetz 2015; vagal tone, can effectively induce analgesia in Oweiss and Badreldin 2015). Such systems have individuals with pelvic pain and reduce blood been used to investigate plasticity mechanisms pressure (BP) in hypertensive patients (Na- in vivo (e.g., Jackson et al. 2006a; Carrillo-Reid padow et al. 2012; Sclocco et al. 2017). et al. 2016), as well as to facilitate adaptive plas- ticity after neural injury (Edwardson et al. 2013; Need for Adaptive Neuromodulation Nudo 2014; McPherson et al. 2015). Responsive CLN systems have also been used in experimen- The requirement for adaptive neuromodula- tal efforts to restore disrupted communication tion arises when a neuromodulation interven- between brain regions in the context of a cogni- tion leads to physiological or clinical effects that tive prosthesis (e.g., Deadwyler et al. 2017), be- are not entirely predictable and that need to tween the brain and the spinal cord (Nishimura be monitored for the parameters of the inter- et al. 2013b; Zimmermann and Jackson 2014; vention to be optimized with regard to those Capogrosso et al. 2016) or the peripheral ner- effects. vous system (Moritz et al. 2008; Bouton et al. In physiological research, an important ap- 2016) in the context of restoration of motor plication of CLN systems is determining stimu- movement is patients with paraplegia or quad- lus-response characteristics of a sensory neural riplegia. circuit by the iso-response method (Gollisch and On a more translational front, “on-demand” Herz 2012). Iso-response curves are trajectories delivery of a neurostimulation-based therapy in the stimulus parameter space that elicit simi- during certain physiological states, inferred by lar neural responses. To explore the parameter physiological and other biomarkers, has two space while no significant changes in the neural main advantages over open-loop delivery: (1) response occur, a CLN system records and quan- higher probability of attaining desirable, state- tifies neural activity in real time, then selects the specific effects, while minimizing the chance of next stimuli so that the neural response remains undesirable side effects, and (2) more efficient on the
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