Sensory stimulation therapy

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Sensory stimulation therapy (SST) is an experimental therapy that aims to use neural plasticity mechanisms to aid in the recovery of somatosensory function after stroke or cognitive ageing. Stroke and cognitive ageing are well known sources of cognitive loss, the former by neuronal death, the latter by weakening of neural connections. SST stimulates a specific sense at a specific frequency. Research suggests that this technique may reverse cognitive ageing by up to 30 years, and may selectively improve or impair two point discrimination thresholds.

Contents

History and motivation

By 2025, it is estimated that 34 million people in the United States will have dementia. It is extremely important, then, that we establish an effective treatment for people with such symptoms to either reduce, or diminish dementia altogether. In modern-day treatment not involving pharmacological treatment, psychosocial therapies are a great intervention. With psychosocial therapies such as massage, aromatherapy, multi-sensory stimulation, music therapy, and reality orientation, treatment of dementia and dementia related diseases has become possible in a less traditional yet non-pharmacological form. [1] It was once believed that the brain was largely unchanging and that its function was decided at a young age. [2] Along this train of thought, cognitive loss from strokes and ageing were viewed as unrecoverable. Functional localization is a theory which suggests that each section of the brain has a specific function, and that loss of a section equates to permanent loss of function. Traditional models even specialize between hemispheres of the brain and describe "artistic and logical sections of the brain." This fatalistic outlook has been dramatically challenged by the recent paradigm of brain plasticity.

Brain plasticity refers to the ability of the brain to restructure itself, form new connections, or adjust the strength of existing connections. [3] The current paradigm allow for conceptualization of brain that is capable of change. Various researchers are using this concept to develop new therapies for conditions that were previously viewed as permanent; for example Paul Bach-y-Rita has worked on devices to give sight to blind individuals, and alleviate a feeling of falling in a patient that has lost function of the vestibular apparatus.

It has been found that many senses have some plastic nature about them. Even auditory cognition has been shown to have some potential for recovery after stroke. A recent study by Sarkamo et al. has shown that listening to music and audio books during early recovery from stroke can result in improved cognition. [4]

This paradigm has opened doors into the previously believed to be impossible; recovery from strokes, reduced cognitive ageing.

Stroke

CT scan slice of the brain showing a right-hemispheric ischemic stroke (left side of image). INFARCT.jpg
CT scan slice of the brain showing a right-hemispheric ischemic stroke (left side of image).

A stroke can be caused by a few different situations, but the basic result is the same. Blood flow to a section of the brain is stopped, which results in rapid depletion of oxygen and other nutrients in the starved section. The starved section of brain tissue quickly begins to die, and results in a lesion in the brain. The resulting lesion can be traced loss of various cognitive functions depending on the location and area of damage. [5]

It is common for stroke patients to suffer from muscle weakness and loss of muscle function. Some natural recovery has been observed, however training based in advances in neuroscience have shown the most dramatic improvements. These investigational therapies focus on repetition of basic tasks with limited appendages. It is generally found that more intensive remedial function therapies result in the greater restoration to function. [6] fMRI and PET scan studies have shown that after as little as 3 weeks of the intensive training programs there are statistical differences between the experimental group and controls, with observable improvements in muscle control. [7] Although these methods have opened doors for improved quality of life for stroke patients, the training methods are very time, and attention intensive. It would be a powerful tool if one could find a system that does not have massive attention requirements.

Cognitive ageing

During ageing, many brain functions decline and some are lost, this is referred to as cognitive ageing. In the most extreme cases one might think about the catastrophic results of Alzheimer's disease. Age is the largest risk factor for Alzheimer's disease. However, due to lack of knowledge and successful research in this field, little is known about the rates of clinical decline and brain atrophy. [1] This disease is associated with neuronal death. However, more general ageing considers loss of synaptic strength over neuronal death. [8] When considering this situation, the machinery for proper functioning of the brain is still present, but is in disarray. It has been shown that as much as a 46% decrease in dendrite spine number and density can occur in humans over 50 years old when compared to older participants. [9]

Somatosensory system

The cortical homunculus, or the visual representation of how your brain sees your body, was discovered by Wilder Penfield Sensory Homunculus.png
The cortical homunculus, or the visual representation of how your brain sees your body, was discovered by Wilder Penfield

The cortical homunculus, or the visual representation of how your brain sees your body, was discovered by Wilder Penfield. a world-famous brain surgeon. Upon ending his career as part of the McGill medical faculty, he served as the director of Neurological Institute.

The somatosensory system is the part of our sensory system that deals with touch. We would not be able to feel things like temperatures, pain, pressure, vibration, and skin rash without the unwavering help of our somatosensory system. [10] The peripheral nervous system has the ability to understand touch, pressure, vibration, limb position, heat, coldness, and pain. This information is sent through the peripheral nervous system, to the spinal cord where it is finally processed by the brain. One of the key structures in processing this information is the primary somatosensory cortex, which is located in the parietal lobe. The primary somatosensory cortex is known to have subsections that process information from different sections, and the area of the cortex for each section is related to its acuity. This observation is often shown symbolically through a homunculus. [11]

Sensory stimulation therapies

Sensory stimulation uses rapid stimulation of nerves in a section of skin to drive neuronal changes in the participant. The nerves are electrically stimulated in a fashion referred to as coactivation. [12] [13] In both cases the participant's limb, often hand, is constrained in a device that has a section that applies the stimulation. The participant is allowed to go about their daily activities, and many do not mind the presence of the device. [12] These degree of reorganization is often measured through two point discrimination thresholds, which measure the smallest distance between two points that can be felt by the subject.

It has been shown that the use of this technique can rest as much as 30 years of sensory loss. [12] In the study by Dinse et al., 28 patients between the ages of 66 to 86 tested similarly to participants 30 years younger than themselves after treatment. These participants had the device attached for 3 hours while undergoing stimulation. Other studies have used shorter periods of stimulation and achieved similar results. [14]

Coactivation

A recent study published in the Archives of Physical Medicine and Rehabilitation followed four patients recovering from strokes while undergoing electrical sensory stimulation therapy. Their progress was followed through several different tests; Touch Threshold, Tactile Acuity, Haptic Object Recognition, Pegs placed in peg board and motor tapping tests. It was found that all patients increased their performance during the study. Although this study uses a small sample group, and had no control group it is a first step study that suggests future studies. [13]

Future studies were developed around this study, in which participant's skin was electrically stimulated to induce signals sent to the brain.

Frequency studies

In January 2008, Ragert et al. explored the impact of frequency of stimulation on sensory stimulation techniques to induce plastic changes. The study investigated if varying the frequency could be used to induce either Long-Term Potentiation (LTP) or Long-term Depression (LTD). LTP refers to the processes by which neuronal connections are formed and strengthened through stimulation and activity. Conversely LTD is a process by which a neuronal pathway is decreased by low levels of stimulation or by disuse. [15]

In the study, Ragert et al. divided their participants into two groups, both of which underwent the SS therapy, but the frequency of stimulation was varied between the two groups. Their analysis showed a statistical improvement in two point discrimination tests for the high frequency group, and a statistical impairment of the same test on the low frequency group. [15] This result brings an interesting possibility to light for the future of this technique; SS could be used to both recover lost sensory function, but also to dull chronic pain.

Activity-dependent plasticity and sensory stimulation therapy

Activity-dependent plasticity refers the phenomenon by which neuronal connections changes via repetitive use. This form of plasticity has been used by neuro-rehabilitation clinics to help those recovering from strokes; for example The Taub Therapy Clinic uses a constraint induced therapy. [2] This therapy focuses on stroke patients with limited function in a limb. The patient's good limb is constrained and the patient is directed through physical tasks of increasing difficulty to induce recovery of neural networks.

The American Stroke Association published an article in 2005 by Sawaki et al. on the possible use of SS to supplement UDP therapies. They suspected that because of the importance of somatosensory information in movement, that enhancing sensory processing through SS could also improve UDP. Their experiment had two experimental groups; both groups were directed to complete voluntary movements with their thumb, and one group underwent 20 minutes of SS before the directed thumb movements. It was found that the paired participants had greater recovery of function. [14]

Impact on cortical maps

Cortical maps are the maps in which parts of our brain, such as the somatosensory system, are described. The cortical maps in our brains do not so much relate to our senses so much as it relates to our sense of physical touch. It has been found that the use of intensive training methods can be used to enlarge cortical maps for patients recovering from a stroke. Studies with that use fMRI and PET scans have shown that the degree of activation increases in the motor cortex of patients undergoing intensive therapies. [16] This provides a strong support to the idea that plastic changes in the brain are a mechanism by which recovery can occur.

Acupuncture and physiotherapy improving postural control

Patients suffering from hemiparetic stroke [17] often lose their ability to stand upright and hold their posture on their own. Without the ability to control our posture, we lose the ability to move freely and voluntarily, which is necessary for activities of daily living (ADL). Studies have been conducted to see if sensory stimulation could improve functionality after a stroke occurs. The study compared two groups; a group undergoing standard physical therapy (group 1), and a group that was given sensory stimulation with acupuncture, physiotherapy, and ADL training (group 2). Both groups began the study within ten days of the initial stroke. Group 2 achieved stimulation via traditional Chinese acupuncture (10 needles), placed according to traditional Chinese acupuncture points and kept in place for 30 minutes. Alongside the manual stimulation, electric stimulation (2 to 5 Hz) was also given to four of the ten needles. The treatment continued for four to ten days, with an average of six and a half days. The twenty-one patients in group 2 had a mean age of 74.2 and the mean age of group 1 was 74.8. From the patients in group 2 which postural recordings could be made, 7 patients suffered from hemiparetic lesion on the left side and 10 had lesions on the right. Of the patients in group 1, 4 had lesion to the left side and 3 on the right. Upon testing, the subjects stood on a platform with their heels together and their arms crossed over their chests. The subjects were exposed to perturbations via vibratory stimulus on their calf muscles, which caused anteroposterior movement, or galvanic stimulation of the vestibular nerves, causing lateral movement. Three different tests were done, with patients eyes both open and closed. [18] Results of the study found that there were major differences in group 1, the control group, and group 2, the treatment group. More patients of the treatment group than the control group were able to maintain a healthy stance during perturbations. As both groups were being treated for post stroke symptoms, it was thought that these perturbations would enhance their posture and motor movements naturally. Among the subjects who survived 2 or more years after hemiparetic stroke, the treatment group (group 2), withheld better postural control. Furthermore, patients who had any additional sensory stimulation were comparable acquired values approaching the normal for age-matched healthy subjects when postural control was measured. The sensory stimulation tests enhanced at least partial recovery of postural function for up to 2 years after the stroke and treatment. After testing, it was deduced that improved recovery after sensory stimulation can be accomplished by patients regaining near normal dynamics of human postural control. Postural control is one of the most important issues in rehabilitation of stroke, thus concluding that sensory stimulation obtained from this study may enhance the functional plasticity of the brain. [18]

Conclusion

Sensory stimulation therapy is a developing technique aimed at recovering sensory loss after strokes and restoring losses from ageing. It has not been proven that sensory stimulation therapy can actually improve brain plasticity, nor cognitive function. The paradigm of brain plasticity marked a fundamental change in the way that the brain is understood, and considered for future therapies. [2] SS takes advantage of this paradigm and the senses are presented with simple stimulation to cause changes inside the brain. In this particular situation a section of skin is stimulated either through electrical or physical means. Signals are sent through the peripheral nervous system to the somatosensory cortex. [12] [13] These signals are then the impetus for changes inside the brain. It has been shown that the adjustment of frequency in this technique can be used to induce either Long Term Potentiation or Long Term Depression. [15] In the case of LTP as much as 30 years of sensory loss has been shown to be recoverable in relatively short time periods. [12] SS has been paired with Use Dependant Plasticity training systems and it has been shown that enhanced recovery is produced from the combination. [14] One of the striking advantages of this technique is that it is not necessary for the participant to pay attention to the stimulus in order to gain benefit from the therapy. [12] This technique opens many interesting doors for future therapies. A potential challenge for this technique is that there is little transfer of gains from one section of skin to another.

Many studies have been conducted, most with some kind of positive conclusion however, further studies need to be conducted sensory stimulation in dementia in order to prove or disprove any theories. [19]

See also

Related Research Articles

A vegetative state (VS) or post-coma unresponsiveness (PCU), is a disorder of consciousness in which patients with severe brain damage are in a state of partial arousal rather than true awareness. After four weeks in a vegetative state, the patient is classified as being in a persistent vegetative state (PVS). This diagnosis is classified as a permanent vegetative state some months after a non-traumatic brain injury or one year after a traumatic injury. The term unresponsive wakefulness syndrome may be alternatively used, as "vegetative state" has some negative connotations among the public.

Cortical maps are collections (areas) of minicolumns in the brain cortex that have been identified as performing a specific information processing function.

<span class="mw-page-title-main">Barrel cortex</span> Region of the somatosensory cortex in some rodents and other species

The barrel cortex is a region of the somatosensory cortex that is identifiable in some species of rodents and species of at least two other orders and contains the barrel field. The 'barrels' of the barrel field are regions within cortical layer IV that are visibly darker when stained to reveal the presence of cytochrome c oxidase and are separated from each other by lighter areas called septa. These dark-staining regions are a major target for somatosensory inputs from the thalamus, and each barrel corresponds to a region of the body. Due to this distinctive cellular structure, organisation, and functional significance, the barrel cortex is a useful tool to understand cortical processing and has played an important role in neuroscience. The majority of what is known about corticothalamic processing comes from studying the barrel cortex, and researchers have intensively studied the barrel cortex as a model of neocortical column.

Multisensory integration, also known as multimodal integration, is the study of how information from the different sensory modalities may be integrated by the nervous system. A coherent representation of objects combining modalities enables animals to have meaningful perceptual experiences. Indeed, multisensory integration is central to adaptive behavior because it allows animals to perceive a world of coherent perceptual entities. Multisensory integration also deals with how different sensory modalities interact with one another and alter each other's processing.

Cerebral atrophy is a common feature of many of the diseases that affect the brain. Atrophy of any tissue means a decrement in the size of the cell, which can be due to progressive loss of cytoplasmic proteins. In brain tissue, atrophy describes a loss of neurons and the connections between them. Brain atrophy can be classified into two main categories: generalized and focal atrophy. Generalized atrophy occurs across the entire brain whereas focal atrophy affects cells in a specific location. If the cerebral hemispheres are affected, conscious thought and voluntary processes may be impaired.

Neuroplasticity, also known as neural plasticity, or brain plasticity, is the ability of neural networks in the brain to change through growth and reorganization. It is when the brain is rewired to function in some way that differs from how it previously functioned. These changes range from individual neuron pathways making new connections, to systematic adjustments like cortical remapping or neural oscillation. Other forms of neuroplasticity include homologous area adaptation, cross modal reassignment, map expansion, and compensatory masquerade. Examples of neuroplasticity include circuit and network changes that result from learning a new ability, information acquisition, environmental influences, practice, and psychological stress.

Michael Matthias Merzenich is an American neuroscientist and professor emeritus at the University of California, San Francisco. He took the sensory cortex maps developed by his predecessors and refined them using dense micro-electrode mapping techniques. Using this, he definitively showed there to be multiple somatotopic maps of the body in the postcentral sulcus, and multiple tonotopic maps of the acoustic inputs in the superior temporal plane.

Body schema is a postural model that keeps track of limb position. The neurologist Sir Henry Head originally defined it as a postural model of the body that actively organizes and modifies 'the impressions produced by incoming sensory impulses in such a way that the final sensation of body position, or of locality, rises into consciousness charged with a relation to something that has happened before'. As a postural model that keeps track of limb position, it plays an important role in control of action. It involves aspects of both central and peripheral systems. Thus, a body schema can be considered the collection of processes that registers the posture of one's body parts in space. The schema is updated during body movement. This is typically a non-conscious process, and is used primarily for spatial organization of action. It is therefore a pragmatic representation of the body’s spatial properties, which includes the length of limbs and limb segments, their arrangement, the configuration of the segments in space, and the shape of the body surface. Body schema also plays an important role in the integration and use of tools by humans.

<span class="mw-page-title-main">Environmental enrichment</span> Brain stimulation through physical and social surroundings

Environmental enrichment is the stimulation of the brain by its physical and social surroundings. Brains in richer, more stimulating environments have higher rates of synaptogenesis and more complex dendrite arbors, leading to increased brain activity. This effect takes place primarily during neurodevelopment, but also during adulthood to a lesser degree. With extra synapses there is also increased synapse activity, leading to an increased size and number of glial energy-support cells. Environmental enrichment also enhances capillary vasculation, providing the neurons and glial cells with extra energy. The neuropil expands, thickening the cortex. Research on rodent brains suggests that environmental enrichment may also lead to an increased rate of neurogenesis.

Activity-dependent plasticity is a form of functional and structural neuroplasticity that arises from the use of cognitive functions and personal experience; hence, it is the biological basis for learning and the formation of new memories. Activity-dependent plasticity is a form of neuroplasticity that arises from intrinsic or endogenous activity, as opposed to forms of neuroplasticity that arise from extrinsic or exogenous factors, such as electrical brain stimulation- or drug-induced neuroplasticity. The brain's ability to remodel itself forms the basis of the brain's capacity to retain memories, improve motor function, and enhance comprehension and speech amongst other things. It is this trait to retain and form memories that is associated with neural plasticity and therefore many of the functions individuals perform on a daily basis. This plasticity occurs as a result of changes in gene expression which are triggered by signaling cascades that are activated by various signaling molecules during increased neuronal activity.

<span class="mw-page-title-main">Somatosensory system</span> Nerve system for sensing touch, temperature, body position, and pain

In physiology, the somatosensory system is the network of neural structures in the brain and body that produce the perception of touch, as well as temperature (thermoception), body position (proprioception), and pain. It is a subset of the sensory nervous system, which also represents visual, auditory, olfactory, and gustatory stimuli.

Extinction is a neurological disorder that impairs the ability to perceive multiple stimuli of the same type simultaneously. Extinction is usually caused by damage resulting in lesions on one side of the brain. Those who are affected by extinction have a lack of awareness in the contralesional side of space and a loss of exploratory search and other actions normally directed toward that side.

<span class="mw-page-title-main">Cross modal plasticity</span> Reorganization of neurons in the brain to integrate the function of two or more sensory systems

Cross modal plasticity is the adaptive reorganization of neurons to integrate the function of two or more sensory systems. Cross modal plasticity is a type of neuroplasticity and often occurs after sensory deprivation due to disease or brain damage. The reorganization of the neural network is greatest following long-term sensory deprivation, such as congenital blindness or pre-lingual deafness. In these instances, cross modal plasticity can strengthen other sensory systems to compensate for the lack of vision or hearing. This strengthening is due to new connections that are formed to brain cortices that no longer receive sensory input.

Cortical stimulation mapping (CSM) is a type of electrocorticography that involves a physically invasive procedure and aims to localize the function of specific brain regions through direct electrical stimulation of the cerebral cortex. It remains one of the earliest methods of analyzing the brain and has allowed researchers to study the relationship between cortical structure and systemic function. Cortical stimulation mapping is used for a number of clinical and therapeutic applications, and remains the preferred method for the pre-surgical mapping of the motor cortex and language areas to prevent unnecessary functional damage. There are also some clinical applications for cortical stimulation mapping, such as the treatment of epilepsy.

<span class="mw-page-title-main">Neuronal recycling hypothesis</span>

The neuronal recycling hypothesis was proposed by Stanislas Dehaene in the field of cognitive neuroscience in an attempt to explain the underlying neural processes which allow humans to acquire recently invented cognitive capacities. This hypothesis was formulated in response to the 'reading paradox', which states that these cognitive processes are cultural inventions too modern to be the products of evolution. The paradox lies within the fact that cross-cultural evidence suggests specific brain areas are associated with these functions. The concept of neuronal recycling resolves this paradox by suggesting that novel functions actually utilize and 'recycle' existing brain circuitry. Once these cognitive functions find a cortical area devoted to a similar purpose, they can invade the existing circuit. Through plasticity, the cortex can adapt in order to accommodate for these novel functions.

<span class="mw-page-title-main">Cortical remapping</span>

Cortical remapping, also referred to as cortical reorganization, is the process by which an existing cortical map is affected by a stimulus resulting in the creating of a 'new' cortical map. Every part of the body is connected to a corresponding area in the brain which creates a cortical map. When something happens to disrupt the cortical maps such as an amputation or a change in neuronal characteristics, the map is no longer relevant. The part of the brain that is in charge of the amputated limb or neuronal change will be dominated by adjacent cortical regions that are still receiving input, thus creating a remapped area. Remapping can occur in the sensory or motor system. The mechanism for each system may be quite different. Cortical remapping in the somatosensory system happens when there has been a decrease in sensory input to the brain due to deafferentation or amputation, as well as a sensory input increase to an area of the brain. Motor system remapping receives more limited feedback that can be difficult to interpret.

<span class="mw-page-title-main">Tactile hallucination</span>

Tactile hallucination is the false perception of tactile sensory input that creates a hallucinatory sensation of physical contact with an imaginary object. It is caused by the faulty integration of the tactile sensory neural signals generated in the spinal cord and the thalamus and sent to the primary somatosensory cortex (SI) and secondary somatosensory cortex (SII). Tactile hallucinations are recurrent symptoms of neurological diseases such as schizophrenia, Parkinson's disease, Ekbom's syndrome and delirium tremens. Patients who experience phantom limb pains also experience a type of tactile hallucination. Tactile hallucinations are also caused by drugs such as cocaine and alcohol.

A cortical implant is a subset of neuroprosthetics that is in direct connection with the cerebral cortex of the brain. By directly interfacing with different regions of the cortex, the cortical implant can provide stimulation to an immediate area and provide different benefits, depending on its design and placement. A typical cortical implant is an implantable microelectrode array, which is a small device through which a neural signal can be received or transmitted.

Gait variability seen in Parkinson's Disorders arise due to cortical changes induced by pathophysiology of the disease process. Gait rehabilitation is focused to harness the adapted connections involved actively to control these variations during the disease progression. Gait variabilities seen are attributed to the defective inputs from the Basal Ganglia. However, there is altered activation of other cortical areas that support the deficient control to bring about a movement and maintain some functional mobility.

Dyschiria, also known as dyschiric syndrome, is a neurological disorder where one-half of an individual's body or space cannot be recognized or respond to sensations. The term dyschiria is rarely used in modern scientific research and literature. Dyschiria has been often referred to as unilateral neglect, visuo-spatial neglect, or hemispatial neglect from the 20th century onwards. Psychologists formerly characterized dyschiric patients to be unable to discriminate or report external stimuli. This left the patients incapable of orienting sensory responses in their extrapersonal and personal space. Patients with dyschiria are unable to distinguish one side of their body in general, or specific segments of the body. There are three stages to dyschiria: achiria, allochiria, and synchiria, in which manifestations of dyschiria evolve in varying degrees.

References

  1. 1 2 Boote, Jonathan; Lewin, Vincent; Beverley, Catherine; Bates, Jane (2006). "Psychosocial interventions for people with moderate to severe dementia: A systematic review". Clinical Effectiveness in Nursing. 9: e1–e15. doi:10.1016/j.cein.2006.06.002. ISSN   1361-9004.
  2. 1 2 3 Norman Doidge (2007). The brain that changes itself: stories of personal triumph from the frontiers of brain science . New York, N.Y: Viking. ISBN   978-0-670-03830-5. OCLC   71189897.
  3. Zhang X; Poo MM (March 2010). "Progress in neural plasticity". Science China Life Sciences. 53 (3): 322–9. doi:10.1007/s11427-010-0062-z. PMID   20596926. S2CID   21508712.
  4. Särkämö T, Pihko E, Laitinen S, et al. (December 2010). "Music and speech listening enhance the recovery of early sensory processing after stroke". J Cogn Neurosci. 22 (12): 2716–27. doi:10.1162/jocn.2009.21376. PMID   19925203. S2CID   14758688.
  5. Hallett M (October 2001). "Plasticity of the human motor cortex and recovery from stroke". Brain Res. Brain Res. Rev. 36 (2–3): 169–74. doi:10.1016/S0165-0173(01)00092-3. PMID   11690613. S2CID   15171827.
  6. Nelles G (2004). "Cortical reorganization--effects of intensive therapy". Restor. Neurol. Neurosci. 22 (3–5): 239–44. PMID   15502268.
  7. Langhammer B; Stanghelle JK (August 2000). "Bobath or motor relearning programme? A comparison of two different approaches of physiotherapy in stroke rehabilitation: a randomized controlled study". Clin Rehabil. 14 (4): 361–9. doi:10.1191/0269215500cr338oa. hdl: 10852/28081 . PMID   10945420. S2CID   42243092.
  8. Hof PR; Morrison JH (October 2004). "The aging brain: morphomolecular senescence of cortical circuits". Trends Neurosci. 27 (10): 607–13. doi:10.1016/j.tins.2004.07.013. PMID   15374672. S2CID   31680049.
  9. Jacobs B; Driscoll L; Schall M (October 1997). "Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study". J. Comp. Neurol. 386 (4): 661–80. doi:10.1002/(SICI)1096-9861(19971006)386:4<661::AID-CNE11>3.0.CO;2-N. PMID   9378859. S2CID   25252374.
  10. Gleveckas-Martens, N. "Somatosensory system anatomy" . Retrieved 13 August 2012.
  11. Dale, Ed Purves (2011). Neuroscience. Sunderland, Mass: Sinauer Associates, Inc. ISBN   978-0-87893-695-3. OCLC   794367770.
  12. 1 2 3 4 5 6 Dinse HR; Kleibel N; Kalisch T; Ragert P; Wilimzig C; Tegenthoff M (July 2006). "Tactile coactivation resets age-related decline of human tactile discrimination". Ann. Neurol. 60 (1): 88–94. doi:10.1002/ana.20862. PMID   16685697. S2CID   6778931.
  13. 1 2 3 Smith PS; Dinse HR; Kalisch T; Johnson M; Walker-Batson D (December 2009). "Effects of repetitive electrical stimulation to treat sensory loss in persons poststroke". Arch Phys Med Rehabil. 90 (12): 2108–11. doi:10.1016/j.apmr.2009.07.017. PMID   19969176.
  14. 1 2 3 Sawaki L; Wu CW; Kaelin-Lang A; Cohen LG (January 2006). "Effects of somatosensory stimulation on use-dependent plasticity in chronic stroke". Stroke. 37 (1): 246–7. doi: 10.1161/01.STR.0000195130.16843.ac . PMID   16322491.
  15. 1 2 3 Ragert P; Kalisch T; Bliem B; Franzkowiak S; Dinse HR (2008). "Differential effects of tactile high- and low-frequency stimulation on tactile discrimination in human subjects". BMC Neurosci. 9: 9. doi: 10.1186/1471-2202-9-9 . PMC   2244613 . PMID   18215277. Open Access logo PLoS transparent.svg
  16. Tegenthoff M, Ragert P, Pleger B, et al. (November 2005). "Improvement of tactile discrimination performance and enlargement of cortical somatosensory maps after 5 Hz rTMS". PLOS Biol. 3 (11): e362. doi: 10.1371/journal.pbio.0030362 . PMC   1255742 . PMID   16218766. Open Access logo PLoS transparent.svg
  17. Takahashi CD; Reinkensmeyer DJ (March 2003). "Hemiparetic stroke impairs anticipatory control of arm movement". Exp Brain Res. 149 (2): 131–40. doi:10.1007/s00221-002-1340-1. PMID   12610680. S2CID   18564943.
  18. 1 2 Magnusson M; Johansson K; Johansson BB (June 1994). "Sensory stimulation promotes normalization of postural control after stroke" (PDF). Stroke. 25 (6): 1176–80. doi: 10.1161/01.STR.25.6.1176 . PMID   8202976.
  19. Collier L; McPherson K; Ellis-Hill C; Staal J; Bucks R (December 2010). "Multisensory stimulation to improve functional performance in moderate to severe dementia--interim results" (PDF). Am J Alzheimers Dis Other Demen. 25 (8): 698–703. doi:10.1177/1533317510387582. PMID   21131677. S2CID   14720189.