Animal models of dystonia

Based in part on some of the findings of altered learning in rodent models, a primate model of dystonia was developed. This model revealed that repetitive stimulation of fingers not normally stimulated together resulted in dystonic postures of the hand and sensory abnormalities. Using electrophysiological methods in the monkeys, the investigators found that the representation of the fingers in the somatosensory cortex was much more disorganized in the dystonic animals after the repetition training than before. This finding is further support for the idea that dystonia results from faulty neuroplasticity and that the electrophysiological mechanisms identified in the rodent may underlie the cause. Clinician-scientists have since extended this to human patients with dystonia and indeed, are finding similar sensory abnormalities in humans with dystonia as those seen in monkeys with learning-induced dystonia. The prevalence of focal dystonia in musicians and other professionals who perform repetitive movements is also consistent with the faulty neuroplasticity hypothesis of dystonia. Behavioral treatments of patients with focal dystonia based on these ideas of learning discovered and understood from work performed in animal models is being met with some success.
There is presently no cure for dystonia. Other than the behaviorally-based treatments used in focal dystonia, the treatments for most cases of dystonia involve drugs that minimize, but do not eliminate symptoms. Moreover, the drugs – those that influence the neurotransmitters acetylcholine or dopamine – used for treatment are often associated with uncomfortable side-effects. Botulinum toxin is used to alleviate symptoms of focal dystonia. The toxin acts to temporarily paralyze the muscles receiving the injection. This helps reduce and even eliminate the sustained muscular contractions and therefore the pain, associated with dystonia. Of course this treatment is temporary and requires repeated injections to maintain effectiveness.
A recent surgical treatment that is being explored for severe cases of dystonia, in which traditional medical therapies do not work, is called deep brain stimulation. In this procedure, stimulating electrodes are placed within the brain at selected locations. The electrodes are attached to a connecting wire that runs from the top of the electrodes in the scalp, behind the ear, down the neck and then attaches to a battery pack called a pulse generator that is implanted under the skin just below the collarbone. This pulse generator provides a constant source of electrical stimulation to the targeted brain region and acts like a pacemaker for the brain, roughly akin to the way pacemakers operate to control the rhythmic activity of the heart.  The video below illustrates on such treatment case.

How did it come about that stimulating the brain with electrical current could alleviate symptoms of disease? After the discovery, using frogs, that nerves and muscles were electrically excitable by Luigi Galvani in 1791, other pioneering researchers began to stimulate the brains of humans and animals using electrical current. Prior to Galvani’s finding, the idea to do this would not have even occurred to anyone. Most notable of the work based on the findings of Galvani, is the work around the same time, of Luigi Rolando, Pierre Flourens in humans and Eduard HitzigGustav Fritsch and David Ferrier in dogs and monkeys. These pioneers discovered that they could use surgical procedures to introduce small electrodes into the brain and provide electrical current to surface and deep brain regions. They also discovered that passing electrical current into the brain influenced behavior and had little side-effects. Victor Horsley and Robert Clarke invented the stereotactic method for neurosurgery. Their method improved considerably the surgical technique of placing electrodes into the brain. Their invention was published in 1906 and is still in use today for human and animal neurosurgery with only slight modifications. Using animals such as cats and monkeys (Walter Rudolf) and a famous bull (Jose Delgado), scientists went on to develop the technique of implanting electrodes into the brain permanently to stimulate deep brain structures. These scientists showed for the first time that electricity could be delivered to the brain of animals and could alter the behavior of the animals, all while the animals were moving around freely. This brought the technique out of the confines of the surgical theatre and opened the door for the possibility of using chronic, deep brain stimulation to treat humans with disease.
In the early 1980s, Irving Cooper boldly introduced electrical stimulation of different regions of the brain in an effort to relieve the symptoms of dystonia in humans. Without the work of scientists such as Ferrier and Delgado showing that the method of electrical stimulation was efficacious and safe in animals first, it is unlikely that Cooper would ever have thought to do this in humans. Initially Cooper targeted areas in the brain such as the internal capsule and the thalamus and indeed, his patients found relief.  Today, deep brain stimulation is used to treat symptoms of dystonia although the regions of the brain are different from those targeted by Cooper. The reason different brain regions are targeted is also based on the confluence of experimental work in animals and clinical work in humans. For example, anatomical work in animals provided scientists and clinicians with a much more detailed wiring diagram of how different brain regions are connected and interact. This has led to the refinement of electrode placement in patients. The clinical experience of surgeons together with detailed follow-up of the outcomes of surgery provides further refinement of electrode placements. Animal studies demonstrated that the effects of the deep brain stimulation propagate throughout the entire basal ganglia-thalamo-cortical system. This appreciation led directly to human studies investigating other potential targets for deep brain stimulation such as the globus pallidus external division and the putamen. Indeed, knowing whether or not the influence and efficacy of deep brain stimulation is due to stimulation of neuronal elements local to the stimulated target or at some distance simply cannot be addressed in humans. Studies such as these with animals, mostly non-human primates, are continuing to provide insight and possibilities into alternative brain structures to target that may have better efficacy or reduced side-effects.
A second area in which animal research has had direct benefits to humans is in understanding how deep brain stimulation works. The original theories about how deep brain stimulation resulted in beneficial effects were based on clinical experiments in humans alone.  Surgeons compared the effects of deep brain stimulation to those of effects of destructive lesions of the same brain areas, such as pallidotomy and thalamotomy.  Based on these comparisons, high frequency electrical stimulation was thought to inhibit or suppress the brain regions that were being stimulated – just like the more permanent lesions would do. Whereas, low frequency stimulation was thought to electrically excite the brain areas.  Thanks to animal research, we now know that this is not the case. Animal studies, including some from our laboratories, demonstrated very clearly that certain neuronal elements were activated with high frequency electrical stimulation.
One powerful example of the confluence of human and animal work that is bearing fruit is to study patients who have received deep brain stimulation treatment to understand the pathophysiological changes in the brain. In this way, abnormal neuronal signatures can be used in the development of animal models of dystonia in the future. We are taking such an approach in our work. In the Basso laboratory we study how the basal ganglia and one of its target structures, the superior colliculus contribute to how we make decisions about where to look. We are particularly interested in how these decisions are made when sensory information is unavailable or ambiguous. We use non-human primates as a model because the brain regions responsible for vision and eye movements are very well-studied in this species and are very similar to those in humans. Indeed, a large amount of the functional magnetic resonance imaging work performed in humans has confirmed the findings discovered in monkeys over the past 30 years. We have found that monkeys will rely on their previous experience or memories to help guide their choices when sensory information is ambiguous or uncertain. We are actively searching for electrophysiological signatures of these processes in the brains of the monkeys. As a next step we are asking, do patients with disease have difficulty making decisions when faced with uncertainty? As it turns out, our preliminary data suggest that patients with the movement disorder Parkinson’s disease do have difficulty making choices when faced with uncertainty. When sensory information is available to guide the decision, the difficulties are less apparent. We are hoping to test patients who have had deep brain stimulation implants soon to assess whether this treatment improves the cognitive symptoms.
Parkinson’s disease is a neurodegenerative disease that results in profound movement symptoms and involves the basal ganglia. Dystonia is different from Parkinson’s disease most notably because dystonia is not associated with neuronal degeneration. Nevertheless, dystonia shares some significant characteristics with Parkinson’s disease. For example, some patients with dystonia show rigidity that is common in patients with Parkinson’s disease. Some patient with Parkinson’s disease show focal dystonias such as blepharospam, a sustained contraction of the eyelid closing muscle. In some patients, the blephparospam can be so severe that the patient is rendered functionally blind. Thus, based on work developed largely within cognitive neuroscience in the non-human primate model, we are planning to extend our cognitive studies to patients who have dystonia and who are being treated with deep brain stimulation. Our goal is to assess the cognitive symptoms seen in these patients and to assess whether deep brain stimulation influences these processes. We can then go back to the laboratory with answers from our human work to explore the development of a monkey model of the cognitive symptoms seen in movement disorders.
As another example, Montgomery is revealing the pathophysiological properties of the human brain circuits in basal ganglia diseases like dystonia and Parkinson’s disease. By extending to humans sophisticated, electrophysiological and statistical techniques that were developed in animals, Montgomery is recording the abnormal electrophysiological signatures of the brains of patients while they are undergoing surgery for the treatment of their disease. These experiments shed light on how the physiological properties in the brain go awry in disease. Most interesting will be to then compare these unhealthy electrophysiological signatures from human brains to those from healthy non-human primate brains to uncover mechanisms of symptoms.
There is still a great deal about dystonia and its treatment that we do not know and it is only with the continued confluence of animal and human neuroscience do we stand a chance of unlocking the mystery and providing relief for patients who suffer from dystonia.

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