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Stimulating brains, altering minds
  1. W Glannon
  1. Walter Glannon, Departments of Philosophy and Community Health Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; wglannon{at}ucalgary.ca

Abstract

Deep-brain stimulation has been used to treat advanced Parkinson disease and other neurological and psychiatric disorders that have not responded to other treatments. While deep-brain stimulation can modulate overactive or underactive regions of the brain and thereby improve motor function, it can also cause changes in a patient’s thought and personality. This paper discusses the trade-offs between the physiological benefit of this technique and the potential psychological harm.

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Electrical and magnetic stimulation of the brain has shown considerable therapeutic promise for a range of neurological and psychiatric disorders. This includes techniques such as electroconvulsive therapy, transcranial magnetic stimulation (TMS), transcranial direct current stimulation, vagus nerve stimulation and deep-brain stimulation (DBS). The most widely used and effective brain-stimulating technique is DBS. Unlike the other techniques just mentioned, DBS involves direct intervention in the brain and thus entails more risks to the patient. Electrodes are surgically implanted in one or more brain regions. The electrodes are connected to a battery-driven stimulator implanted in the chest near the collarbone that can be switched on and off remotely through the skin. Activation of the electrodes stimulates the relevant sites in the brain.

Most neurological and psychiatric disorders involve dysregulation in cortical, limbic and subcortical regions of the brain. The effects of TMS, for example, are limited because it stimulates only the cortex, and the strength of the magnetic field it generates falls off sharply beyond a few centimetres from the stimulated site. DBS is superior to TMS and other forms of stimulation for neurological and psychiatric disorders because of its modulating effects on cortical-thalamic and cortical-limbic circuits in the three general brain regions. This explains why it has been medically indicated for and used with varying degrees of success to treat Parkinson disease (PD), essential tremor, depression, chronic pain, obsessive-compulsive disorder and Tourette syndrome.1 Although DBS involves more risks than non-invasive or less invasive forms of brain stimulation, it has fewer risks than ablative neurosurgery, where any damage to the brain can be permanent. Unlike the surgical lesions made to correct dysfunctional brain circuits, DBS is adjustable and reversible. The settings of the electrodes and the stimulator can be changed. Alternatively, the stimulator can be turned off, and the implanted electrodes can be removed from the brain. Nevertheless, because DBS is brain-invasive and does have risks, it is and likely will continue to be offered only to patients with the most severe and intractable disorders that have not responded to any other treatments. The purpose of all forms of neurostimulation is to modulate underactive or overactive brain regions mediating motor control and mental states associated with cognition and emotion.

Stimulating the brain may improve physiological and psychological symptoms of some conditions. Yet it may alter a range of mental states critical to thought, personality and behaviour. This can disrupt the integrity and continuity of the psychological properties that constitute the self and one’s experience of persisting through time as the same person. As an interdisciplinary group of European neuroscientists, philosophers and legal theorists led by Reinhard Merkel point out:

Practically no intervention in the structure or functioning of the human brain can be undertaken in complete certainty that it will not affect mental processes, some of which may come to play a key role in a person’s self-concept.2

The uncertainty is a function of the fact that it is not known exactly how electrical or magnetic stimulation alters brain activity. It is not known which targets in the brain are optimal for producing salutary effects on motor, cognitive and affective functions. Nor is it known at what frequency the stimulation should be delivered to produce these effects, which can vary among different patients.

I discuss actual effects of DBS on the mind and how they influence decisions by patients and physicians about whether to have, forgo, continue or discontinue this treatment. I present a case involving a neurological disorder to generate and frame discussion of the psychological and ethical aspects pertinent to three related questions: how do patients and their physicians weigh the potential benefit against the potential harm of this intervention in the brain? How much alteration of one’s thought and personality in treating a neurological or psychiatric disorder with DBS would be consistent with a patient’s rational choice to undergo the procedure? How much alteration of the patient’s mind would be consistent with a neurologist’s or psychiatrist’s duty of care to the patient?

EMPIRICAL EVIDENCE: BENEFITS AND RISKS

DBS has been effective in controlling motor symptoms associated with advanced PD. Its target is two subcortical structures in the basal ganglia critical for motor function, the globus pallidus interna and the subthalamic nucleus. DBS is now considered standard of care for treating PD in some medical centres. It can enable patients to have more control of their condition, not only because the device can improve motor function, but also because patients can operate the device on their own outside of a clinical setting. For some patients, the procedure has a more favourable benefit-risk profile and thus is preferable to drugs such as dopamine agonists, which can cause addiction and other types of compulsive behaviour.3 The drugs can overcompensate for dopamine depletion in the basal ganglia, which has been implicated as one cause of the disease.

DBS is not without risks, however. In one study, this technique caused symptoms in patients similar to those associated with dopamine agonists. They became impulsive in their decision-making, displaying impairment in their capacity to consider all options before choosing and acting.4 One explanation of this phenomenon is that stimulating the basal ganglia interferes with the functions of prefrontal cortical areas of the brain, which ordinarily regulate deliberative behaviour. Drugs such as levodopa may control some motor symptoms but may also cause motor fluctuations, dyskinesias and impair some forms of learning. Yet alternatives such as DBS can inappropriately accelerate decision-making in some patients and interfere with their autonomy. This is just one example of the trade-offs between physiological benefit and psychological harm in treating PD.5 There are physiological risks as well, including haemorrhage and infection at the site where the electrodes are implanted and stimulated.6 DBS also has significant risks when used for psychiatric disorders. A recent study of subthalamic nucleus stimulation for severe obsessive-compulsive disorder involving 18 patients resulted in 15 severe adverse effects overall.7 These included one intracerebral haemorrhage and two infections. The main psychiatric adverse event was hypomania, which resolved after adjustment of the stimulator. This indicated that the stimulation was causing this psychiatric state. In a study using DBS targeting the subcallosal cingulate gyrus for treatment-refractory depression, 12 out of 20 patients had significant improvement in their symptoms, effectively going into remission for one year.8 Yet an earlier study of this technique targeting the subgenual cingulate for depression indicated that it could cause hypomania and amplification of the effects of antidepressants.9 There were also reports of rebound depression when the stimulator was turned off.

Given that DBS can result in both beneficial and harmful effects in individuals with PD, how do we weigh these different effects in determining whether the procedure can be justified? Because the adverse effects on the mind can be significant, and because these effects are not predictable from one patient to the next, a full complement of medical professionals should be involved in deliberating these questions with the patient. These would include neurologists, neurosurgeons and anesthesiologists directly involved in the procedure, as well as psychiatrists, psychologists, social workers and family members to explore the potential impact of the procedure on the patient. This involves not only deliberating whether to offer the procedure, but also monitoring its effects in determining whether it should be continued.10 Whether medical professionals should offer DBS for this disorder depends on their assessment of benefit and risk. But ultimately it is the mentally competent patient who has to decide whether the effects of DBS would be acceptable and whether he or she should have it.

On one level, the decision hinges on a comparison between the physical benefit of motor control and the potential psychological harm of an adverse change in thought, personality and behaviour. On a deeper level, the decision hinges on a question involving a comparison between two psychological states: whether the emotional suffering from loss of motor control is worse than changes in other states of mind. The key factor is the patient’s quality of life and whether DBS yields a net benefit in this respect. The medical trade-offs between the positive physical and negative cognitive and emotional effects of drugs versus electrical stimulation, or stimulation versus no treatment, also involve ethical trade-offs between different types and degrees of psychological harm.

A CASE STUDY

We can gain insight into this problem by considering a case of a patient from The Netherlands who received DBS for advanced PD.11 Three years after the implantation of electrodes in the subthalamic nucleus and the start of DBS, a 62-year-old male was admitted to a psychiatric hospital for a manic state caused by the stimulation. A mood stabiliser failed to control his symptoms, which included megalomania and chaotic behaviour that resulted in serious financial debts. He became mentally incompetent. Adjustment of the stimulator resolved the mania and restored his cognitive capacity for insight and rational judgment. Yet this resulted in a return of his motor symptoms, which were so severe that the patient became bedridden. This left the patient and his healthcare providers with a choice between two mutually exclusive options: to admit the patient to a nursing home because of a serious physical disability, despite intact cognitive and affective capacities; or to admit the patient to a chronic psychiatric ward because of a manic state, despite restoration of good motor function.

In this case, DBS produced the desired effect of motor control. But it also had the adverse effect of a significant alteration of the patient’s state of mind. When his brain was not being stimulated, he was considered competent to decide about his own treatment, and he chose the second option. In accord with his competent expressed wish, he was legally committed to a chronic ward in a regional psychiatric hospital. This clearly was a choice between two undesirable options, a choice that he made on quality-of-life grounds. Assuming that he had the capacity to compare the two states, loss of motor control was worse than mania. He chose to continue DBS because the net benefit of being on the stimulator was greater than being off it. Or more accurately, the net harm of stimulation was less than the net harm of stopping it. It was the lesser of two evils. The psychological effect of stimulating the brain in this case is more extreme than the impulsivity mentioned earlier. Yet both cases illustrate how DBS can modulate some brain circuits only to overexcite others and result in psychopathology.

This case raises three main questions. First, by choosing an option that would leave him in a manic and thus mentally incompetent state, would he be waiving his autonomy, specifically regarding his capacity to consent to continuation or discontinuation of DBS and thus the ability to change his mind? Second, given that his choice would radically alter his state of mind, should this influence the decision of the medical team to continue stimulating his brain? Third, if his thought and behaviour significantly changed as a result of brain stimulation, then how could be benefit from it? Each of these ethical questions hinges on the differences between positive physiological and negative psychological effects of a medically indicated treatment

AUTONOMY AND IDENTITY

The patient’s decision in this case seems similar in some respects to an advance directive made by a competent patient regarding subsequent medical treatment decisions that will have to be made when he or she is no longer competent to make them. This occurs most commonly in cases of dementia such as Alzheimer disease and usually pertains to end-of-life care. Advance directives allow competent individuals to state the interests they will have over the course of their lives. They can foresee how their bodies and minds will deteriorate over time, which medical interventions would be consistent with their interests, and which surrogate decision-makers would best respect these interests.12 Formulating an advance directive also gives one control over one’s life by limiting decisions and actions by others that can affect one when no longer competent.

The PD case at issue here is different from the loss of decisional capacity in a typical application of an advance directive in at least two respects. Because the stimulator causes the patient to experience mania when it is turned on, the loss of decisional capacity is not a gradual or subsequent development but immediate. He autonomously and knowingly chooses an option that immediately makes him mentally incompetent and devoid of decisional capacity. The immediate loss of agency distinguishes this case from the gradual loss of agency in Alzheimer disease.13 Moreover, unlike the demented patient, whose condition in irreversible, this patient’s mental incompetence is reversible because the mania can be stopped by turning off the stimulator. While the patient’s decision has the effect of binding him to state of mental incompetence, it is not his intention in opting for stimulation. The mania is an undesirable but acceptable side effect of the realisation of his intention to relieve the suffering he experiences in his loss of motor control. Yet his decision would have the effect of precluding any possibility of changing his mind. Paradoxically, an autonomous decision to consent to a medical treatment would make him lose his autonomy and capacity to subsequently choose to continue this treatment and to have or forego others.

Some might question whether the patient is competent enough to make an autonomous decision.14 His affective state in response to his loss of motor control may impair his capacity to rationally consider the implications of his decision to continue with the stimulation. Antonio Damasio has shown that cognitive and affective capacities are interdependent and sustained by interacting cortical and limbic pathways in the brain. Impairment in either of these capacities may interfere with practical and moral reasoning and decision-making.15 Yet there is no obvious affective impairment in the PD patient when he decides to resume the stimulation. Even if he were slightly depressed, this by itself would not imply that he lacked decisional capacity. As Paul Appelbaum has convincingly argued, depression by itself does not undermine decisional capacity.16 A depressed patient may retain a sufficient degree of decisional capacity to understand the consequences of having or forgoing DBS. Nor would any feeling of desperation necessarily mean that the patient’s decision was irrational or not sufficiently informed.

Although the patient has exercised his autonomy in consenting to the continuation of DBS for his disease, he need not be so constrained by his decision. Before initiating the procedure, his physicians would be obligated to discuss options that would not foreclose possible future actions that could benefit him. Changing the settings of the stimulator might resolve the mania problem. In the light of this possibility, when the patient made his decision the medical team caring for him would be obligated to offer to revisit the question of whether to continue or discontinue DBS at a later time. This would mean stopping the stimulation so that mental competence could be restored and the patient and his treating physicians could discuss treatment options. In this way, the medical team would be providing conditions allowing the patient the fullest expression of his autonomy in consenting to or refusing an intervention consistent with his own all-things-considered best interests. All of these steps would fall within the medical team’s obligation to monitor the patient’s condition over an extended period of time. Yet if the patient competently refused the future option of discontinuing stimulation in order to reassess whether to continue or discontinue this treatment, his decision would have to be respected.

The psychological continuity in virtue of which one persists as the same person over time can accommodate some changes in one’s mental states.17 It can accommodate some degree of change in the integrated set of experiences and memories that form one’s identity. The concept of identity at issue here is not numerical identity, the idea that an individual at a later time T2 is the same as an individual at an earlier time T1. This condition can be satisfied by a minimal set of physical and psychological properties. Rather, the relevant concept of identity in this case is narrative identity. This consists of the characteristics and experiences that make up the distinctive autobiography of a person.18 These characteristics include the set of dispositional traits we refer to as personality. But how much change in one’s mental states can an individual undergo and remain the same person? How much disruption can one’s life narrative accommodate without threatening the integrity of the whole? Is there a threshold of continuity and integrity below which alteration of the psyche is substantial enough to alter the identity of the person? (Merkel 2007, chpt 5).3 Gradual and subtle changes in personality are less likely to disrupt the necessary degree of integration of mental states to retain identity. But this may not be the case when there is a sudden radical change between earlier and later mental states. If the mania alters the general content and disrupts the integrity and continuity of his desires, beliefs, intentions and emotions, then the PD patient seems to become a different person once the stimulator is turned on. The mania produced by the DBS may put this patient below the threshold. So even when a medical procedure is effective, can it be justified if it radically alters one’s life narrative and effectively turns one into a different person?

Neurosurgery generally involves more risks in altering thought and behaviour than DBS. Resecting a diffuse brain tumour is a delicate procedure that may damage healthy brain tissue and result in loss of language ability, memory, vision or significant changes in personality. Different surgeons and patients will be prepared to accept different degrees of risk. How much risk both parties are willing to accept depends on the probability of biological survival and the patient’s quality of life with or without surgery. Although biological survival is not a factor in deciding whether to continue stimulating the brain for advanced PD, the risk of substantial changes to the psyche is. The trade-off is between acceptable quality of life regarding motor control and alteration of the mind. One comes at the cost of the other. The question of justifiability in the case under discussion is significant because the mania that alters identity is not just a probable but a certain result of stimulation.

For the patient, an alteration of his self resulting in less suffering is preferable to a self with more suffering. To be sure, not every patient would have this same preference. Freud had a painful oral cancer for many years that required a series of mouth and jaw operations. Yet he refused to take anything stronger than aspirin until the very end. He reportedly said, “I prefer to think in torment than not to be able to think clearly”. Retaining a state of mind that allowed him to remain aware of his surroundings and to interact with others was more important than relief of his pain with narcotics, which would have altered this state.19 The contrast between Freud and the PD patient illustrates how weighing the positive and negative effects of a drug or procedure on the psyche can be quite different from one person to the next.

One might question how an individual could benefit from a treatment if his or her identity changes as a result of it. If the alteration of mental states is substantial, then it is unclear who the beneficiary of the treatment would be. The individual experiencing the positive effects of the treatment would appear to be a different person from the one who requested the treatment. Still, the manic state of the PD patient does not entail a complete disruption of psychological continuity. This mental abnormality would appear to disrupt the thematic unity of the total set of his mental states over time and thus disrupt his narrative identity. But mania alone would not necessarily preclude his capacity to recall what it was like to lose motor control and to experience the positive effect of restoring this control. In spite of the change from a non-manic to a manic state, there may be enough psychological continuity and narrative integrity for him to retain a weaker yet sufficient sense of identity to remain the same person. Even if there is a substantial change in his identity following the brain stimulation, the moment he experiences relief from his suffering is enough to plausibly say that he benefits from it. The stimulation satisfies his interest in restoring motor control.20 This point shows that metaphysical and psychological questions of identity cannot be separated from the normative question of benefit versus harm. The possibility of changes to the patient’s psyche must be contextualised by the goal of relieving his suffering. Applying Ronald Dworkin’s distinction, the patient’s experiential interests supersede his critical interests. The satisfaction he experiences in regaining motor control outweighs any interest he may have had in pursuing more general values and commitments in his life.21

The Benelux Neuromodulation Society recommends that

DBS of STN (subthalamic nucleus) for Parkinson disease should not be abandoned because of potential risks for behaviour and cognition. For the time being, extensive preoperative psychiatric and neuropsychological screening and special attention for cognitive and behavioural changes during follow-up seems to be warranted.10

The discussion of the case of the 62-year-old with PD suggests that we can go even further and make a stronger claim. Some individuals with neurological disorders suffer from them and desire symptom relief to such a degree that they would be willing to undergo or continue treatment entailing the risk of significant unwanted side effects on the psyche. Indeed, some individuals would be willing to make this choice when these effects were not just probable but certain. Some degree of desperation may motivate their decision. But desperation by itself does not mean that a patient lacks mental competence and decisional capacity, or that this would be an irrational choice for the patient. If the upshot of discussion of treatment options by the patient and the medical team is that the net benefit of DBS outweighs the net harm, then the decision to continue stimulation can be in the patient’s best interests and accordingly ethically justified.

CONCLUSION

Electrical stimulation of subcortical regions of the brain can control and relieve physical and psychological symptoms of a number of neurological and psychiatric disorders. For many patients, however, this involves trade-offs between positive and negative effects on the mind. The technique may effectively treat symptoms associated with a disorder only to cause adverse psychological effects, which may not be predictable. More controlled studies can help to get a clearer sense of the general safety and efficacy of DBS. On this basis, researchers and clinicians can better inform patients with these disorders, or their surrogates, about the relative benefits and risks. Yet no two persons’ brains are alike, and no two persons’ minds respond in the same way to treatments affecting the brain. A physiological improvement does not always translate into a psychological benefit for a person undergoing an intervention in the brain. What counts as a successful medical treatment for a neurologist or psychiatrist does not necessarily mean that the patient is better off as a result of it. Medical professionals and patients together need to consider the effects of DBS on the brain and the mind. In the end, though, it is the competent patient who has to decide whether the trade-offs in any given treatment would be acceptable and whether he or she should have or continue to have it.

Acknowledgments

I am grateful to the two JME reviewers for their comments.

REFERENCES

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Footnotes

  • Funding: The writing of the paper was supported in part by the Canadian Institutes of Health Research, NNF 80045, States of Mind: Emerging Issues in Neuroethics.

  • Competing interests: None.

  • Provenance and peer review: Not commissioned; not externally peer reviewed.

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