A science communication project about conditional rewarding brain stimulation


Deep brain stimulation (DBS) is increasingly applied to the ventral striatum, a key region in the brain's reward system, in order to help patients who suffer from depression [R,R,R,R], obsessive-compulsive disorder [R,R,R,R,R,R] and other psychiatric conditions [R,R]. DBS of the reward system could also be used as a reinforcer ('rewarding brain stimulation', RBS) to motivate challenging behaviours, such as physical exercise [R,R] and learning [R,R]. However, the use of RBS in human patients is associated with serious concerns regarding safety and ethics [R,R], and has a controversial history [e.g. R]. iPlant.eu is a science communication project aimed at analysing these concerns as they appear in public opinion. The project is organized around the concept of an iPlant - a hypothetical DBS system for motivating certain challenging but beneficial behaviours. A range of opinions about the iPlant were collected and analysed. Three categories of concern were identified: access control, government misuse, and damage to health or self-discipline. The outcome of the project was presented at the International Neuromodulation Society conference in 2009 [R,L].

Video from the International Neuromodulation Society conference in 2009

iPlant.eu is written and maintained by Christopher Harris and is licensed under a Creative Commons License (Attribution - NonCommercial - ShareAlike). Attribution/citation: 'Harris, C.A. and Kilarski, L.L. (2009) A Novel, Web-Based Approach To Public Participation in Neuromodulation Research. 9th World Conference of the International Neuromodulation Society.' For up-to date information about the iPlant project, rewarding DBS and related topics, follow iPlant on Twitter, Facebook or YouTube. Please address comments and questions about the iPlant project to christopher@iplant.eu.

References: R = academic, L = website


Deep brain stimulation (DBS). DBS is a surgical procedure in which electrodes are chronically implanted deep in the brain in order to modulate neural activity [L,L]. The operation takes 8-12 hours and costs about $40.000, not counting the additional cost of regular follow-ups and battery replacement. Complications include bleeding, infection, electrode misalignment and damage to brain tissue during surgery. Most DBS implants are used to treat refractory Parkinson's disease, tremor and dystonia. More recently however their use has been extended to psychiatric disorders, including depression [R,R,R,R] and obsessive-compulsive disorder [R,R,R,R]. In these cases, electrodes are implanted in the ventral striatum, a central component of the brain's reward system.

The reward system. The brain's reward system is a network of neurons involved in the attribution of value. This system is essential for attention, motivation, learning and volontary movement [R,R]. Central to the reward system are dopaminergic (dopamine-producing) neurons located near the middle of the brain in the ventral tegmental area and substantia nigra (Figure 1). Destroying these neurons or blocking their activity severely impairs goal-seeking behaviour and learning [R]. Dopaminergic neurons extend axons into the frontal cortex, striatum and hippocampus (Figure 1). The ventral striatum (particularly the subregion called the nucleus accumbens) receives very substantial dopaminergic inputs and is a central node in the reward system [R]. Release of dopamine into target brain regions reinforces ongoing neural activity [R,R] and synaptic connectivity [R,R]. The dopaminergic neurons are themselves activated by input from multiple brain regions [R]. These inputs determine the what an animal finds rewarding or valuable. Rewards such as food and sex are associated with sharply increased realease of dopamine [R] whereas low dopamine concentrations are associated with distractability and a lack of motivation [R].

What is dopamine?, Dopamine and the frontal lobes, Spontaneous and dopamine-driven brain activity

Dopamine on Facebook

Rewarding brain stimulation (RBS). Activation of the reward system by current incjection is refered to as rewarding brain stimulation (RBS) or brain stimulation reward. Targets for stimulation include the dopaminergic cell bodies, their axons as they project to the forebrain along the medial forebrain bundle, and their target regions (e.g. ventral striatum) [R,R,R]. Optogenetic activation of dopaminergic neurons is similarly rewarding [R,R,R]. RBS raises dopamine concentrations in the brain sharply, particularly in the striatum and frontal cortex [R,R,R], and animals work very hard to receive it. Rats for example forgoe natural rewards such as food and sex if given the opportunity to induce RBS by pressing a lever [R,R]. RBS can therefore be used to motivate animals to perform challenging behaviours. Rats will run on treadmills, lift wheights and solve problems to recieve RBS, and perform better than rats recieving natural rewards [R,R,R]. Other species respond similarly to RBS [e.g. R].

What is rewarding brain stimulation?

RBS in the human brain. Early attempts to use RBS as a medical treatment were discontinued [R,R], but demonstrate that the human brain too responds to RBS. When given the opportunity to self-stimulate one patient "stimulated himself to a point that, both behaviourally and introspectively, he was experiencing an almost overwhelming euphoria and elation and had to be disconnected, despite his vigorous protests" [R]. Today DBS is again being applied to the reward system [R,R,R,R,R,R,R,R,R,R,R,
R] but the current that is applied is constant and deliberately set at an intensity that induces only moderate feelings of happiness [R]. A constant state of euphoria (mania) would obviously be maladaptive and dangerous. However, strong RBS could be applied conditionally in order to motivate specific, challenging behaviours, as discussed below. The increasing use of DBS to target the reward system (particularly the ventral striatum), combined with the potential health benefits of, for example, artificially motivated physical exercise, suggest that the implications of using conditional RBS to motivate human patients need to be considered. The aim of the present project is to analyse public opinion about these implications.

How Happy Is Too Happy?


The iPlant. The concept of an 'iPlant' was developed here as a shorthand for a hypotehtical DBS system designed to motivate challenging but beneficial behaviours, such as physical exercise, learning or research (see below). The purpose of this neologism was to organize public engagement and discussion around a concrete example of how DBS could be used to motivate challenging behaviours. Specifically, the iPlant is defined as delivering RBS whenever a specific behaviour is performed, thus enhancing a person's motivation to continue that behaviour. It is assumed that patient and doctor would agree, under stringent medical and legal supervision, which behaviour would be rewarded and how performance of that behaviour would be monitored. For example, in order to motivate execise, RBS could be delivered whenever a patient uses a rowing machine or when pressure-sensitive sensors in his or her shoes hit the ground during running. The health benefts of regular physical exercise [e.g. R] might for certain patient groups outweigh the risks associated with DBS surgery, for example in the treatment of morbid obesity. (Note that that DBS of the hypothalamus has already been attempted in order to reduce feelings of hunger in morbidly obese patients [e.g. R].) An iPlant could similarly be used to deliver RBS whenever a patient provides correct answers to questions designed to provide training in languages, mathematics etc. Such an application could be useful for persons suffering from severe learning disabilities. Much more speculatively, iPlants might eventually be used to motivate the simpler and more repetitive aspects of laboratory research.

What is an iPlant?, iPlant seminar

iPlant on Facebook

Public engagement. A variety of text and video material describing the iPlant and associated concepts was created and made available for comment online. Most of this material is still available on various sites including on YouTube, the IEET website, and on various blogs [e.g. L,L]. A forum was created for more in-depth discussion. In addition, people wrote direct emails and posted thoughts about iPlants on their own blogs [e.g. L,L,L,L,L,L]. By analysing this public engagement with the iPlant concept we aimed to gain a better understanding of problems associated with conditional RBS and of how those problems might be addressed in accordance with public opinion. Written comments were collected and used in an ongoing manner to develop the communication project, e.g. to identify and address frequently recurring statements and questions.

Results and discussion

Comments regarding the possibility of using of DBS to motivate challenging but benificial behaviours generally fell into one of four categories: positive, concern about access control, concern about government misuse and concern about damage to health or self-discipline (Figure 2). The following data are based on a sample of 145 comments collected in June and July of 2009.

Positive. Positive comments expressed general enthusiasm about iPlants, ideas about how to promote their development, and occasionally a desire to personally use such technology. About 22% of comments were positive.

Concern about access control. The three categories of concern all hinge on the fact that iPlants depend fundamentally on RBS being delivered if and only if a pre-specified beneficial behaviour is performed. Several commentors highlighted the risk that patients might find ways to circumvent such restrictions and self-stimulate unconditionally and endlessly, or that malicious individuals might find ways to circumvent restrictions and take control of the behaviour of another person. Use of iPlants would therefore clearly require that patients have limited access to the settings of their implants, that such limitations are subject to very effective enforcement, and that an accountable regulator (e.g. a doctor, hospital or implant manufacturer) is able to maintain access control without abusing the trust of the patient. About 17% of comments expressed concern about access control.

Concern about government misuse. The second category of concern highlights the risk that, even with robust access control, governments or cultures might misuse iPlants by motivating citizens to engage in demeaning or dangerous behaviour, by for instance forcing individuals to conform to unreasonable standards of productivity. These concerns indicate that development of iPlants should only take place in the context of transparency and public debate, and under the oversight of appropriate medical and civil rights groups such as the UN's International Bioethics Committee [L]. Some 27% of comments were about the potential for government misuse.

Concern about damage to health or self-discipline. The third category of concern is about the negative impact artificial motivation could have on patients' health or self-discipline. For example, a person who exercises one hour per week before being fitted with an iPlant would theoretically be able to exercise much more frequently with the aid of RBS but would also be tempted to always use the implant for motivation when exercising. Removing the one weekly hour of "iPlant-free" exercise might be psychologically damaging since regular exertion of effort is necessary to maintain natural self-discipline. This indicates that RBS-motivated behaviour should only be engaged in when the patient would otherwise be idle or engaged in destructive behaviour. This category of concern also included a range of other health risks. Again the ability for hospitals to ensure safe, effective and beneficial use of the implant technology appears to be a key issue. About 15% of comments expressed concern about self-discipline or other aspects of health. The remaining 19% of comments expressed general interest, neutrality, existential concerns, or simply called for more public debate about iPlants.

Conclusion and future directions

Implanting electrodes deep in the brain is difficult, costly and involves a nontrivial risk of permanent disability. The idea of using RBS to motivate challenging but beneficial behaviors in human patients will therefore not be relevant to the vast majority of people until such time as DBS implants and the necessary surgical procedures become as safe and cost-effective as for example plastic, dental or laser eye surgery. Improved biocompatibility of DBS implants and better use of robot-assisted surgical techniques may accelerate this developent. Less invasive ways of stimulating the brain include transcranial magnetic stimulation, ultrasound, and even heat. These methods lack the depth, precision and power of DBS, but may improve in the future. It may also be possible to use gene therapy to improve the motivation-related functions of the ventral striatum [R]. Despite these caveats, conditional RBS remains the only method by which patients today could be fully motivated to perform challenging behaviors. In some cases - in for example the treatment of morbid obesity - the benefits to the patient may outweigh the risks of DBS surgery.

This possibility raises a number of questions in addition to the three categories of concern discussed above. What legal challenges would have to be overcome for a conditional RBS treatment to be attempted in a hospital? What would a team of surgeons have to do to get approval for such a treatment? How should the patient-doctor agreement be formulated and enforced? How would doctors decide the appropriate amount of current/motivation needed to perform a particular behavior (non-conditional DBS of the reward system involves a similar problem [R])? Which behaviors would the implants be used to motivate? Further work is needed to answer these questions and to address the three identified categories of concern.

Key references

Malone et al. (2009) Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol Psychiatry 65(4):267-75.

Burgess et al. (1991) Intracranial self-stimulation motivates treadmill running in rats. J Appl Physiol. 71(4):1593-7.

Bichot et al. (2011) Stimulation of the nucleus accumbens as behavioral reward in awake behaving monkeys. J Neurosci Methods 199(2):265-72.

Hermer-Vazquez et al. (2005) Rapid learning and flexible memory in "habit" tasks in rats trained with brain stimulation reward. Physiol Behav. 84(5):753-9.

Synofzik et al. (2012) How Happy Is Too Happy? Euphoria, Neuroethics, and Deep Brain Stimulation of the Nucleus Accumbens. AJOB Neuroscience 3(1).

Oshima and Katayama (2010) Neuroethics of deep brain stimulation for mental disorders: brain stimulation reward in humans. Neurol Med Chir (Tokyo). 50(9):845-52.

Harris and Kilarski (2009) A Novel, Web-Based Approach To Public Participation in Neuromodulation Research. 9th World Conference of the International Neuromodulation Society.