The International Neuromodulation Society defines neuromodulation as the alteration of nerve activity through the delivery of electrical or electromagnetic stimulation, chemical agents or light (optogenetics) to targeted sites of the central or peripheral nervous system. The aim of neuromodulation is to modulate (aka normalize) pathological nerve function. Some examples of various means to provide âneuromodulationâ to treat various illnesses and symptoms are functional electrical stimulation, spinal cord stimulation, peripheral nerve stimulation, intrathecal drug delivery systems, occipital nerve stimulation, motor cortex stimulation, repetitive transcranial magnetic stimulation, sacral nerve stimulation, transcranial direct current stimulation, vagus nerve stimulation and deep brain stimulation (DBS).
Thus, it appears that electricity has been and still is the main agent used to provide âneuromodulationâ, starting in antiquity with the electrical fish and gaining a momentum with the so-called âelectrotherapyâ in the 18th and 19th centuries when electrotherapy was used for the âtreatmentâ of a variety of illnesses, including epilepsy, paralysis, chorea, deafness, blindness, rheumatism, glandular enlargement and also for artificial respiration and resuscitation [2].
According to the web site of the International Neuromodulation Society (http://www.neuromodulation.com/brief-history-of-neuromodulation consulted on 14 January 2014), âThe modern era of neuromodulation began in the early 1960s, first with deep brain stimulation which was soon followed (in 1967) by spinal cord stimulation, both for otherwise intractable painâ. In the opinion of this author, this is a rather selective way of writing history! In fact, the modern era of neuromodulation began at least a decade before âthe early 1960sâ and it was not âfor otherwise intractable painâ. It is true that the main application of deep brain stimulation in the late 1960s and 1970s was for the treatment of chronic pain, and it is true that Medtronic trademarked the term âDBSâ with respect to chronic subcortical stimulation for pain in the mid-1970s [3]. However, scholar sources show that the history of deep brain stimulation before it was called âDBSâ, that is, the history of electrical stimulation of subcortical structures delivered through chronically implanted electrodes, started in the early 1950s soon after the introduction of the method of human stereotactic surgery. It is also evident that subcortical brain stimulation was not initially intended to treat pain but rather was applied in psychiatry and to modify behaviour. In order to be able to fully grasp the âlessons learned for current practiceâ, as is suggested by the title of this chapter, one has to understand how DBS unfolded historically and why do we today need, in the first place, to âlearn lessonsâ from the âhistory of neuromodulation in psychiatryâ.
In the contemporary discourse about the history of DBS, there is a commonly held belief that DBS was initiated for surgical treatment of movement disorders in 1987 [4], and entered the realm of psychiatry first in 1999 [5, 6]. Indeed, it was the paper by Veerle Vandewalle et al. on DBS for Tourette syndrome published in The Lancet in February 1999 [5], and the publication of Nuttin et al. on DBS for obsessiveâcompulsive disorder (OCD), also in The Lancet in October 1999 [6], that heralded the most recent era of DBS in psychiatry. As the field of psychiatric neuromodulation has literally exploded in the last decade, at least judging by the number of publications in the field, with new psychiatric applications of DBS on an ever-increasing number of brain targets [7], perhaps a sober look at past experience in this field may provide some clues about what is to be expected and what can go wrong in this specific area of psychiatric neuromodulation, aka psychiatric surgery.
The main aim of this chapter is thus to review the historical applications and trials of DBS in the realm of psychiatry and behaviour, and to summarize what lessons, if any, can be learned from these previous practices.
The birth, rise and fall of the 20th-century psychiatric DBS
Human stereotactic neurosurgery was initially and purposely devised with the intent to avoid the devastating side effects of the crude frontal lobotomy by allowing to perform anatomically focused tiny lesions in psychiatric patients. Thus, in the same way, as human stereotactic ablative surgery was applied at its inception in 1947 in the psychiatric domain [8], human subcortical brain stimulation was also first proposed in the realm of psychiatry: in 1952, neurophysiologist and neurobehaviourist JosĂ© Delgado and his colleagues [9] described a technique of electrode implantation for chronic recording and stimulation to evaluate âits possible therapeutic value in psychotic patientsâ. The following year, the Mayo Clinic organized a symposium on âintracerebral electrographyâ. The proceedings of that meeting were published and included a paper on âNeurosurgical and neurologic applications of depth electrographyâ, where one could read: âAn observation that may have some practical significance was that several of our psychotic patients seem to improve and become more accessible in the course of stimulation studies lasting several daysâ [10]. The authors thought that a likely explanation for this effect âwas that the local stimulation was having a therapeutic effect comparable to that of electroshockâ and concluded that â⊠this aspect of localized stimulation studies requires further investigation since it may lead to a most specific, less damaging, and more therapeutically effective electrostimulation technic than can be achieved by the relatively crude extracranial stimulation methods in use at presentâ [10]. One of the authors in this paper was Carl Wilhelm Sem-Jacobsen, a Norwegian neurophysiologist and neuropsychiatrist who was a fellow at the Mayo Clinic and who continued to work with chronic subcortical stimulation for psychiatric illness when he returned to Norway (see further next).
Also in the early 1950s, a team at Tulane University in New Orleans, led by psychiatrist Robert Heath, had started chronic depth electrode stimulation, including stimulation of the âseptal areaâ in schizophrenic and other psychotic patients [11].
Furthermore, already in 1961, Daniel Sheer, Professor of psychology at the University of Houston, edited a book entitled Electrical Stimulation of the Brain â An Interdisciplinary Survey of Neurobehavioral Integrative Systems [12]. As the title indicates the main focus of electrical stimulation was on neurobehaviour and the authors of the chapters of that book discussed the use of subcortical recording and stimulation in epilepsy, obesity, aggressive behaviour and other neurological and behavioural conditions. Hence, from its very beginning, the technique of chronic stimulation of deep brain structures was intended and applied for behavioural and psychiatric studies and occasionally in the treatment of mental disorders.
What went wrong?
Studying the literature on old psychiatric DBS from the mid-1950s to the 1970s, it appears that DBS was used more for exploration and modification of behaviour, and less for the treatment of true psychiatric illness: those scarce publications detailing the few attempts to treat psychiatric illnesses with DBS were authored mainly by neurosurgeons, whereas the non-neurosurgeons were more prolific publishers on DBS mainly as a means to study and alter personality. To give few examples: in 1972, Mexican neurosurgeon Escobedo et al. [13] implanted quadripolar electrodes bilaterally in the head of the caudate nucleus in two patients with epilepsy, mental retardation and destructive aggressive behaviour, and described vegetative, motor and behavioural responses to stimulation. In 1979, West-German neurosurgeon Gert Dieckmann [14] performed unilateral stimulation of the non-dominant thalamus using a quadripolar Medtronic âdeep brain stimulation electrodeâ to treat a woman with phobia. The electrode contacts extended over 12 mm and were aimed at the parafascicular and rostral intralaminar areas. Stimulation was delivered intermittently at a low frequency (5 Hz) and resulted in disappearance of the phobias, while attempts at stimulation with 50 Hz âwas experienced as being very disagreeableâ. A possible reason for the scarcity of neurosurgical papers on psychiatric DBS as a treatment of psychiatric illness during the 1960s and 1970s was that during that period, which saw the demise of the previously popular lobotomy, focused stereotactic ablative procedures (anterior capsulotomy and cingulotomy) were gaining momentum and were the preferred surgical method to treat psychiatric illness, since the DBS hardware and technology of that period were quite cumbersome and not user-friendly.
On the other hand, there is a wealth of publications on DBS from the 1950s through the 1970s, authored by very few psychiatrists and neurophysiologists, in which DBS was not mainly a tool to treat psychiatric disease, but rather to study the brain and to alter human behaviour, as stated earlier. The scholar literature reveals three main workers, a neurophysiologist, a psychiatrist and a neurophysiologist-psychiatrist, who, independently of each other, devoted much of their career to study the effect of DBS in humans and sometimes to promote its use for aims beyond psychiatric disease.
JosĂ© Delgado, a Spanish neurophysiologist and neurobehaviourist who moved from Spain to Yale University in 1950 and worked there with Fulton, is probably best known for a motion picture showing a bull whose charge in the arena could be stopped through remote brain stimulation. Delgado worked extensively with chronic subcortical stimulation in rats, goats and monkeys and then in humans. In a lecture delivered in 1965 titled Evolution of Physical Control of the Brain, he reported: âMonkeys may learn to press a lever in order to stimulate by radio the brain of another aggressive animal and in this way to avoid his attackâ. Heterostimulation in monkey colonies demonstrates the possibility of âinstrumental control of social behaviourâ [15]. He concluded, âAutonomic and somatic functions, individual and social behaviour, emotional and mental reactions may be evoked, maintained, modified, or inhibited, both in animals and in man, by electrical stimulation of specific cerebral structures. Physical control of many brain functions is a demonstrated factâŠâ [15]. Delgadoâs enthusiasm for this new technology and its possible effects on behaviour led him to publish in 1969 a book titled Physical Control of the Mind: Towards a Psychocivilized Society [16]. This bookâs title provoked a storm of critic and Delgado was compelled to negate the impression that mind control could be achieved by electrodes wired into peopleâs brain. He emphasized that the technique of âElectrical Stimulation of the Brain (ESB)â, as he called it, was meant as a research tool to study and understand the human mind. Delgado then developed a technique of subcortical stimulation using chronically implanted electrodes connected to a subcutaneous receiver implanted in the scalp that he labelled âStimoceiverâ, which could be remotely controlled by radio waves. This technique of âradio communication with the brainâ was developed by Delgado explicitly for use in psychiatric patients [16â18], although there are no testimonies in the scholar literature to its results in ârealâ patients. Anecdotically, Harvard physician turned writer Michael Crichton described in his semi-fictive and famous book The Terminal Man first published in 1972 [19] a patient whose personality and behaviour were changed by stimulation through several electrodes implanted in various parts of his brain initially for control of epilepsy, but who also suffered from psychosis. Some of the stimulation effects experienced by the hero of this novel bear strange resemblance to the DBS experiments conducted on real people by another psychiatrist, Robert Heath, at Tulane University in New Orleans.
Robert Heath was a psychiatrist at Tulane University, New Orleans. He implanted a multitude of electrodes in several subcortic...