Sensory stimulation programs have a long history of being used in neurorehabilitation, as they are one of the most commonly used treatment options for addressing global disorders of consciousness after severe brain injury .
These programs are based on the idea that enriched environments enhance neural plasticity and therefore improve recovery inbrain-injured patients[2, 1]. However, several recent systematic reviews[3, 4, 5, 6], including one published by the Cochrane Collaboration, concluded that there is still a lack of reliable evidence to support or rule outthe effectiveness of sensory stimulation in patients with global disorders of consciousness (coma, vegetative state or unresponsive wakefulness syndrome, and minimally conscious state).
Additionally, in recent years there have been advances in knowledge about the brain in general and disorders of consciousnessin particular, with new paradigms and theoretical notions emergingto evaluateif the main characteristics of the sensory stimulation method are still appropriate in terms of what we know today.
In 2014, Frontiers in Human Neuroscience published an article  in which the authors reviewed the main characteristics of sensory stimulation with the aim of evaluating which were out-of-date and which were not, while proposing some changes in light of recentfindings and theoretical views.
Today’s blog post briefly discusses sensory stimulation and the current concept of consciousness and disorders of consciousness (DOC), and then gives way to a summary of this work.
Current concept of consciousness and global disorders of consciousness
Traditionally, the state of consciousness and the disorders of consciousness (coma, vegetative state or unresponsive wakefulness syndrome, and minimally conscious state) have been defined based on two factors:
- Arousal (level of alertness; “being conscious”)isthe ability to wake up and maintain the sleep-wake cycle.
- Awareness (content of consciousness; “being aware”)is theability to integrate different sensory stimuli into a knowledge that allows us to be aware of ourselves and our surroundings.
Acomais usually a temporary state in which there is neither arousal nor awareness. Comatose patientsremain with their eyes closed and do not respond to stimulation or communication; in avegetative state, patients’ eyes may be open, which demonstrates preservation of the ascending reticular activating system, and therefore,preserved arousal. However,since they are incapable of generating responses, they lack awareness. Finally, patients in aminimally conscious statecan generatevariable but reproducibleresponses, and thereforepossessawareness in addition to arousal .
However, in recent years, consciousness mechanisms have been associatedto new concepts such as distributed information , interacting cortical areas and brain connectivity [10, 11]. At present, consciousness is viewed as the capacity of a system to integrate informationand it seems to depend on the brain’s ability to support complex activity patterns distributed among interacting cortical areas .
In line with this perspective, disorders of consciousness have recently been redefined as adisconnection syndrome, in which a functional and/or structural circuit-level disruption of acortico-striatopallido-thalamocorticalmesocircuitimpairs the recovery of consciousness, an opinion supported by multiple recent lines of evidence .
Under this connectionist paradigm, new theoretical notions come into play and it is therefore also pertinent to consider new factors when planning the ideal treatments for patients with disorders of consciousness, both at a global level—with regard tothe possible combination of the different existing treatment approaches (neuromodulation, pharmacological treatment, sensory stimulation, etc.)—and at a local level—in respect to each of these approaches, in this particular case, sensory stimulation programs.
What is sensory stimulation? Basis and main characteristics
Sensory stimulation for patients with disorders of consciousness is a methodology aimed at promoting arousal and behavioral responsivenessby the application of environmental stimuli , so that by gradually providingthe patient nervous system with sensory information, the patient is able to perform some actiondepending on their level ofresponsiveness .
For this purpose, sensory stimulation programs use different smells and flavors of moderate-to-high intensity, verbal and non-verbal sounds (e.g., white noise or music), visual stimuli (e.g., objects, photographs) and tactile stimuli (e.g., physical contact, feeling one’s body, feeling objects of different textures, moving objects, etc.).
Although different procedures have been adopted for this method, they invariably include stimuli with the following characteristics :
- Are simple.
- Are administered with a moderate-to-high intensity.
- Are possiblyautobiographical and/or emotional.
- Are repetitive and frequent.
- Are administered under multiple sensory channels.
Sensory stimulation is a low invasive, non-threatening, inexpensive, and simple to apply methodology, and for these reasons, it remains an attractive rehabilitation method .However, as mentioned above, its theoretical basis has not been clearly formulated in the past, and in general, there are contradictory results regarding its effectiveness which require further research of its procedures through a more controlled methodology [3, 4, 5, 6], as well as updating its characteristics according to current findings .
New sensory stimulation options for disorders of consciousness
Abbate et al. evaluated the main featuresof the sensory stimulation standard methodand suggested some possible modifications for its improvement:
Complex stimulation involving structured and meaningful stimuli
As the authors point out, sensory stimulationstandard protocols usually use simple and often meaningless (decontextualized) stimulations, following the tacit hypothesis that patients with disorders of consciousness have reduced attention capacities and therefore, simple stimuli might be more appropriate because they are less demanding in terms of cognitive processing.
However,recent studies indicate that DOC patients can be engaged in structured tasks and may have preserved complex responses, therefore suggesting islands of preserved high-order cognitive functioning.
Based on these findings, the authors propose that the target of future protocols should be the stimulation of these islandsof preserved high-order cognitive functioning, for which a complex stimulationcould be more efficient than a simple one.
Avoid repetitive and frequent stimulations
Sensory stimulation standard programs usually consist of presenting a repetitive, frequent, and moderate-to-high intensity simple stimulation.
The authors stress that this procedure is contrary to the aim of promoting cognitive processing, since it may lead to thehabituationof the response, which, as they recall, is a decrement in neuronal and behavioural response resulting from repeated stimulation.
Therefore,the authors suggestavoiding not only repeated but also frequent presentationof stimuli, as more frequent stimulation also results in more rapid and/or more pronounced response decrement.
Includestimulations with proper intensity, occasionally interspersed with intense stimuli
Regarding intensity, the advantage of high-intensity stimulation (stimuli with sharp onsets and strong energy) is that they can easily activate attention mechanisms. However,given the mixed results of the research in this regard, the authors question whether habituation can also emerge or not with intense stimulation, and therefore propose to combine stimulation of proper intensity with occasional intense stimulation.
Integrated and simultaneous multisensory stimulation
A typical sensory stimulation approach usually involves the stimulation of many different sensory modalities (e.g., visual, auditory, tactile, etc.), that is why it is defined as multimodal. However, stimuli used are unimodal in nature and sensory channels are stimulated one by one. Thus, the stimulation is not really multisensory since different unimodal stimuli are implemented serially.
As the authors note, recent research in multisensory integration suggests that attention tends to orient more easily toward sensory inputs that possess multisensory properties and that this happens automatically.
The authors also mention different research studies in neurophysiology that suggest brain cortical processing is multisensory not just in associative cortices but also in primary cortices, therefore concluding that multisensory stimuli are a better option than unimodal stimuli because they are potentially better at capturing DOC patients’ attentional sources and in engaging their preserved island of high-order cognitive functioning.
Based on studies published since 2005, the authors conclude that stimuli with emotional salience are a valuable option for sensory stimulation procedures.
In particular, authorsinclude findings about: the privileged access that emotional stimuli haveto cognition (attention and awareness);stimuli with emotional contentare better recalledthan stimuli without emotional content;the influence of emotional salience on high-level representations such as thoughts and actions; and the possibility of integration of emotional processing with top-down factors such as attention, task context and conscious awareness.
According to recent research, stimuli with autobiographical content are also a valuable and proper options since, based on the evidence mentioned above, autobiographical memories could promote integration and thus,consciousness, while encompassing the same advantages from emotional processing.
In particular, autobiographical memories engage a large network of brain regionsand accordingly involve multiple memory processes (episodic memory, personal semantic knowledge) and other processes (visual imagery,emotional processing, self-referential and control executive processes), which suggests that these memories facilitate the integration of information.
The close relationship between episodic memory and a high level of consciousness (“autonoetic” consciousness) has also been proposed as a mechanism facilitating consciousness.
Promote behavioral responses by asking the patient to perform actions
Sensory stimulation standard methods are usually limited to stimulate perception, or at most the memory and emotional processing associated with some stimuli.
Based on functional neuroimaging and neurophysiologic studies that have recently shown that a subset of patients with disorders of consciousness exhibit “covert responses”, the authors suggest that it may be beneficial to invite the patient to perform complex actions during the session, so that in addition to promoting arousal, definite behaviors couldalso be promoted through repetitions and exercises.
Although evidence indicates that virtually every experience (perception included) has the potential to alter the brain and produce enduring changes, this plasticity is in many cases specific. Therefore, stimulation limited to perception couldlead tocircumscribed changes, while larger outcomes would be expected by stimulating both the input (perception) and the output (action) processing.
In addition, a theory of action representation has been proposed which regards the action as the core of larger representational networks (with which the authors suggest that an approach addressing actions in addition to perceptions could promote integration).
Naturalistic and dynamicactions in real or virtual situations
(Clinical) settings where stimulation sessions usually take place areartificialand predispose the therapist to use simple and repetitive stimuli that are administered in a controlled manner similarly to how it would occur at a laboratory; moreover, these stimuli often lack emotional salienceand autobiographical content, and are aimed only to stimulate the input processing.
The authors recommend naturalistic, dynamic actions in more appropriate contexts that allow patients to experience situations involving specific behavioral scripts (e.g., having breakfast with the family).
Naturalistic tasks, whether in real or virtual situations, involve complex stimuli and require both input (perception) and output (action) processing. According to the authors, they are ideal backgrounds for introducing emotional and autobiographical stimuli.
Therefore, the possible directions for the future of sensory stimulationproposed by these authors are based mainly on the concept of complex stimulation, which would involve the use of structured and meaningful stimuli that would be delivered to multiple sensory channels in a simultaneous and integrated manner. It would also addressboth input and output cognitive processing, and the performance of dynamic and naturalistic actions that would avoid meaningless repetitive and frequent stimulations, including stimulations with proper intensity which would occasionally be interspersed with intense stimuli.
All of these actions would maintain the valid aspects of emotional salience and autobiographical relevance.
By: Lidia García Pérez
If you liked this article written by the neuropsychologist Lidia García Pérez about new sensory stimulation treatment options for patients with disorders of consciousness, you might find the following interesting as well:
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- Schnakers C & Monti MM (2017). Disorders of consciousnessafterseverebraininjury: therapeuticoptions. CurrOpinNeurol, 30(6): 573-579. doi: 10.1097/WCO.0000000000000495.
- Abbate C, Trimarchi PD, Basile I, Mazzucchi A, Devalle G (2014). Sensorystimulationforpatientswithdisorders of consciousness: fromstimulation to rehabilitation. Frontiers in Human Neuroscience, 8: 616. doi:10.3389/fnhum.2014.00616.
- Lombardi FFL, Taricco M, De Tanti A, Telaro E,Liberati A (2002). Sensorystimulationforbraininjuredindividuals in coma orvegetativestate (Review). Cochrane Database of SystematicReviews, CD001427. DOI: 10.1002/14651858.CD001427.
- Lancioni GE, Bosco A, Olivetti Belardinelli M, Singh N N, O’Reilly M F and Sigafoos J(2010). Anoverview of interventionoptionsforpromotingadaptivebehavior of personwithacquiredbraininjury and minimallyconsciousstate. Dev. Disabil. 31, 1121–1134. doi: 10.1016/j.ridd.2010.06.019.
- Klingshirn H, Grill E, Bender A, Strobl R, Mittrach R, Braitmayer K, Müller M. (2015). Quality of evidence of rehabilitationinterventions in long-termcareforpeoplewithseveredisorders of consciousnessafterbraininjury: A systematicreview. J RehabilMed.47(7):577-85. doi: 10.2340/16501977-1983.
- Padilla R &Domina A (2016). Effectiveness of SensoryStimulation to Improve Arousal and Alertness of People in a Coma orPersistentVegetativeStateAfterTraumaticBrainInjury: A SystematicReview. Am J OccupTher., 70(3):7003180030p1-8. doi: 10.5014/ajot.2016.021022.
- Federación Española de Daño Cerebral (FEDACE) (2011). Cuadernos FEDACE sobre daño cerebral adquirido: síndrome de vigilia sin respuesta y de mínima conciencia. Madrid: FEDACE.
- Gibson RM, Owen AM, Cruse D (2016). Brain-computer interfaces forpatientswithdisorders of consciousness. Progress in BrainResearch,228, pp. 241-291.
- Tononi G. (2004). Aninformationintegrationtheory of consciousness. BMC Neurosci. 5:42. doi: 10.1186/1471-2202-5-4.
- Laureys S (2005). The neural correlate of (un)awareness: lessonsfromthevegetativestate. Sci. 9, 556–559. doi: 10.1016/j.tics.2005.10.010.
- Rosanova, M., Gosseries, O., Casarotto, S., Boly, M., Casali, A. G., Bruno, M.-A., et al. (2012). Recovery of cortical effectiveconnectivity and recovery of consciousness in vegetativepatients. Brain 135, 1308–1320. doi: 10.1093/brain/awr340
- Schiff ND. (2010). Recovery of consciousnessafterbraininjury: a mesocircuithypothesis. TrendsNeurosci., 33:1-9
- Giacino JT(1996). Sensorystimulation: theoreticalperspectives and theevidenceforeffectiveness. Neurorehabilitation 6, 69–78. doi: 10.3233/NRE1996-6108.
- Abbate&Mazzucchi (2011). “La riabilitazioneneuropsicologicadeidisturbiglobalidellacoscienza,” in La RiabilitazioneNeuropsicologica, ed A. Mazzucchi (Milano: MassonElsevier),389–406.