Abstract
BACKGROUND:
The application of emotional stimuli is beneficial when practicing tasks that must be learned.
OBJECTIVE:
This scoping review examined related literature to identify the applicability of emotion-based training for therapeutic activities.
METHOD:
All relevant literature published as of April 1, 2020 in four prominent databases was searched (CINAHL, Embase, PubMed, and PsycINFO) using the five-stage review framework proposed by Arksey and O’Malley.
RESULTS:
After sophisticated searches and exclusions, ten publications were included for further review. Our results revealed three types of emotion-based stimulation methods that can influence therapeutic effects on stroke patients. However, the research did not compare the difference between the pros, cons, and effectiveness of each type of sensory stimulation.
CONCLUSION:
Rehabilitation specialists are encouraged to obtain a broad understanding of therapeutic situations and their possible impacts on a given environment.
Introduction
Emotions are important human factors that have a major impact on occupational performance (Matthews, Paulus, Simmons, Nelssen & Dimsdale, 2004). In particular, the application of emotional stimuli is beneficial when practicing tasks that must be learned. Recent studies suggest that appropriate emotion-based stimulation can enhance both cognitive and physical functioning (Schel & Crone, 2013).
In general, the beginning of emotional changes can be confirmed by the activation of amygdalae in the human brain regardless of the apparent dissimilarities between these emotional changes, such as laughing or crying. In other words, attentive emotional changes activate the amygdalae (Grabowska et al., 2011). Appropriate emotional stimuli attract or divert attention and trigger a variety of subjective and autonomous responses without affecting the work (Lang & Bradley, 2010; Ursache, Blair, Stifter & Voegtline, 2013). However, not all aspects are enhanced by emotion-based training, and some studies indicate that it can induce false memories (Dehon, Larøi & Van der Linder; Grassi-Oliverira, de Azevedo, Carlos & Stein, 2011; Kensinger, 2009), that is, the provision of emotional stimuli can have both positive and negative effects during training.
Emotions are very important factors that affect several environmental stimuli when attempting to optimize a patient’s behavioral performance. They serve as important mediators between human internal conditions and specific situations (Buratto et al., 2014; Kirshner, Weiss & Tirosh, 2016). Recently, evidence from behavioral and neuroimaging studies of patients with brain injuries confirmed that the emotional contents of stimuli provide behavioral motivation and exhibit strong behavioral patterns (Grabowska et al., 2011).
Many researchers have developed rehabilitation protocols for stroke patients; however, further discovery and development of contemporary methods should continue. The introduction of additional influencing factors may produce strong synergistic effects in treatment. In previous studies, emotional stimulation was found to be a motivating factor that could affect explicit behavior, cognitive processing, and consciousness. In addition, this was expected to be a factor that could significantly impact new therapeutic protocols for subjects with limited cognitive and motor functioning due to brain injuries (Blakemore, Shoorangiz & Anderson, 2018; Naugle, Hass, Bowers & Janelle, 2012; Oren, Soroker & Deouell, 2013).
Most reviews of the relationship between emotion-based training and the restoration of human functions did not focus on the possibility of applying them for therapeutic purposes in rehabilitation environments. This scoping review of the literature provides an overview and analysis of previous research to determine the direction of available studies and to suggest further studies. Therefore, the primary purpose of this paper was to examine existing literature to identify the applicability of emotion-based training for therapeutic activities.
Methods
Scoping reviews provide answers to specific questions rather than assessing an entire body of literature. They survey the literature, synthesize quantitative data about what has been achieved in previous studies, and then summarize and interpret the literature of a particular research field. To date, there have been no systematic reviews of this topic because the provision of emotion-based training to patients with brain injuries is a relatively new concept.
Stage 1: Identifying the research question
Each database was searched for studies published as of April 1, 2020, using the five-stage review framework proposed by Arksey and O’Malley. In the first stage, relevant research was reviewed, and three initial exploratory research questions were selected as follows: (1) How have the therapeutic effects of emotion-based training been explained over the past ten years? (2) What are the singularities of past methodologies and results? (3) What is the prevalent direction of the research, and what should be considered when proceeding in the field?
Stage 2: Identifying relevant studies
In the second stage, we established the following eligibility criteria: (1) journal article type, (2) articles published from 2008–present, (3) articles written in English, and (4) studies aimed at confirming the effects of emotion-based stimulation on stroke patients. We combined the following search terms: (emotion OR affective OR motivation OR positive OR negative OR pleasure OR unpleasure) AND (visual stimuli OR visual stimulus OR visual stimulation OR auditory stimuli OR auditory stimulus OR auditory stimulation OR olfactory stimuli OR olfactory stimulus OR olfactory stimulation) AND (stroke OR CVA OR cerebrovascular accident OR hemiplegia OR brain attack OR neglect OR motor impairment OR balance OR limb OR extremity). Studies involving humans and those written in English were used as limits. Four electronic databases were included: CINAHL, Embase, PubMed, and PsycINFO. The pertinent articles were exported and managed using the RefWorks referencing software program.
Stage 3: Study selection
In the third stage, initial selection was performed by reviewing the titles and abstracts. The complete studies were then read and evaluated subject to the eligibility criteria. As the intention was to achieve maximum specificity, this review did not include studies in which the participants had other underlying pathological problems. Studies were also excluded if they had been published as a poster, book, magazine, or were not written in English.
Stage 4: Charting the data
From the final ten articles, data were extracted in seven categories that were used to analyze the full reviews: country, study design, participants, brain damage, emotion-based stimuli, significant stimuli, and the main findings of the analyses. Data extraction was performed independently by the reviewer. A flow diagram illustrated the process of the study selection, and the findings were presented with a narrative description in table form (Tables 1, 2, and 3).
Description of different emotion-based stimulations for rehabilitation training
Description of different emotion-based stimulations for rehabilitation training
IAPS: International Affective Picture System.
Description in rehabilitation training with emotion-based stimulation
Summary of study characteristics and key results from 10 studies
APA: Anticipatory Postural Adjustments, BD Group: Brain damage group, BP: Blood pressure, BPD: Black pepper oil, COP: Center of Pressure, d’: Discriminability, DBP: Diastolic BP, DW: Distilled water, GSR: Galvanic Skin Response, HC: Healthy Condition, HF: High Frequency, HR: Heart Rate, LBD: Left Brain Damage, LBT: Line Bisection Test, LF: Low Frequency, LI: Laterality index, LVO: Lavender oil, MCI: Mild Cognitive Impairment, mTBI: mild Traumatic Brain Injury, n.s.: Not significant, PD: Parkinson disease, PST: Picture Scanning Test, RBD: Right Brain Damage, SCR: Skin Conductance Response, SCT: Star Cancellation Test.
In the final stage of the survey, data were systematically categorized and organized using a data charting form developed using Microsoft Excel (Table 3). The suggestion regarding availability was to treat persons with brain injuries through emotion-based stimuli treatment.
Results
The literature survey yielded a total of 882 citations, of which 425 documents with duplicate titles were eliminated. After the first screening of the titles and abstracts of these articles, 82 studies were considered eligible for further review. Their complete articles were reviewed, after which another 72 studies were excluded because they were either not directly related to emotion-based stimulation (n = 37), did not relate to treatment (n = 23), or did not include patients with strokes (n = 12). Ten studies were used for data analysis (Fig. 1).

Flowchart illustrating the inclusion process.
The literature from four databases was searched for articles published between 2008–2020. Four papers included a randomized controlled trial (RCT), and six were conducted as single group studies. Four used visual and auditory stimuli for emotion-based training, and two used olfactory stimuli. To compare the effects of emotion-based training on therapeutic activities, five papers compared visual perception functions for neglect patients (Chen, Tsai, Huang & Lin, 2013; Grabowska et al., 2011; Grandjean, Sander, Lucas, Scherer & Vuilleumier, 2008; Oren, Soroker & Deouell, 2013; Soto et al., 2009), two compared cognitive ability components (Buratto et al., 2014; Cameirão, Faria, Paulino, Alves & i Badia, 2016), three compared arm, hand, and balance functions (Cameirão et al., 2016; Gim et al., 2015; Iokawa, Kohzuki, Sone & Ebihara, 2018), one compared the characteristics of verbal functioning (Bakhtiyari et al., 2015), and one described more than one effect (Cameirão et al., 2016). A target group with stroke diagnoses was included. Emotion-based training considered the emotional aspects applied to promote learning when performing training tasks.
Thematic summary of the articles
A thematic analysis of the articles revealed the functional characteristics and effects of emotional stimulation utilized for therapeutic training purposes with stroke patients. Each stimulation was further described by classifying the application strategy (Tables 1, and 2). The results are summarized by topic, and the order of the factors does not indicate any specific relevance or priority.
Visual stimulation
In studies of emotion-based training for stroke patients, the use of emotion-based picture cards was shown to affect a patient’s visual perception and memory. The international affective picture system (IAPS) is widely used for emotion-based stimulation. It was used as a stimulus in all of the reviewed studies. There were differences in the number of cards utilized in each study, but there were no significant differences in the applied methods.
In a study of effects that may improve the cognitive abilities of stroke patients, Buratto et al. (Buratto et al., 2014) found that the use of emotion-based picture cards affects a patient’s true and false memory. Specifically, the location of brain lesions can be an important variable for therapeutic effects. Cameirao et al. (Cameirão et al., 2016) explained that the application of virtual reality-based visual stimulation affects upper limb functioning and cognitive ability in stroke patients. They found that negative targets had negative effects on upper extremity and cognitive function, while positive targets had positive effects on a patient’s cognitive functioning. Grabowska et al. (Grabowska et al., 2011) suggested that negative emotional stimuli can affect the visual perception of stroke patients. In addition, functional magnetic resonance imaging (fMRI) was used to analyze responses to visual stimuli provided on the left and right sides. Visual stimuli to the left induced activation of the visual area, but stimuli to the right could have confirmed simultaneous activation of the limbic structure along with the visual region. Oren et al. (Oren, Soroker & Deouell, 2013) found that negative emotional stimuli can cause more lateralization of visual perception in stroke patients. They also showed that positive emotional stimuli caused a “rebalancing” of patients’ visual perception.
Auditory stimulation
Auditory stimulation is often described as a method to increase therapeutic effects in stroke patients with reduced cognitive abilities. In this study, emotion-based auditory stimulation was evaluated as one of the most effective methods for subjects experiencing unilateral neglect. Chen et al. (Chen et al., 2013) demonstrated the possibility of mitigating neglect symptoms when listening to unpleasant music or pleasant music that was preferred over white noise conditions. Pleasant music not only increased awareness of the left area—which is ignored in tasks related to visual search—but also promoted the movement of the left eye in functional visual searches. According to Grandjean et al. (Grandjean et al., 2008), positive or negative emotion-based auditory stimulation can enhance the visual perception of patients with unilateral neglect caused by stroke. In addition, MRI analyses found that emotion-based auditory stimulation contributes to the activation of parietal and temporal regions. Soto et al. (Soto et al., 2009) reported the effectiveness of using music preferred by the subject when performing training tasks. Preferred music had a positive effect on the patients’ visual recognition and reading tasks. This suggests that the provision of positive emotional stimulation to patients may be more effective. It can also be said that this is a meaningful result of explaining the task-based influence rather than the effect on a simple task.
Olfactory stimulation
The effects of olfactory stimulation on functional recovery in stroke patients were identified in two articles. In the study by Gim et al. (Gim et al., 2015), lavender oil was more effective in balance training for patients than black pepper stimulation. The positive emotion-based olfactory stimulus could have produced a significant effect on the relatively challenging task performance. In the study by Iokawa et al. (Iokawa, Kohzuki, Sone & Ebihara, 2018), lavender and grapefruit oil stimulation produced higher stability when performing upper limb tasks than distilled water. Although the functional effect of the task was not clearly defined, the change could have been confirmed by using the patient’s biological parameters when performing the upper limb-based task. As a result, this suggests that the influences of environmental stimuli should be considered. An uncomfortable treatment environment may negatively affect the patient’s rehabilitation training and require placement of the patient in a treatment room according to the patient’s unique characteristics.
Discussion
This scoping review aimed to provide an overview of the effects of emotion-based stimulation that contribute to functional improvements during the training process when treating stroke patients. A total of ten publications focusing on the study of treatment effects were included, and the main subjects were stroke patients. The results of our review revealed three types of emotion-based stimulation methods that could affect therapeutic effects on stroke patients. However, none of the studies compared the differences between the pros, cons, and effectiveness of each type of sensory stimulation. For example, in the studies by Buratto and Grandjean (Buratto et al., 2014; Grandjean et al., 2008), for the emotion-based stimulation provided through visual and auditory stimuli that explained the therapeutic effects of each emotion, there were no further insights regarding how and why the effects differed between application methods. It was striking that most of the studies lacked the perspective of interventions to improve motor skills in the upper and lower extremities of stroke patients. In general, given the prevalence of disabilities experienced after stroke, it was surprising that only a few studies approached this factor. As the present study was not intended to investigate the overall quality of the reviewed studies, readers should not perceive the results as definitive proof of effects; instead, they should interpret this as a suggestion to carefully consider emotional stimulation in the treatment of stroke patients. Several synonyms and approximations were combined in the review filters to include as many relevant publications related to emotion-based stimulation as possible. Publications that related to other neurological diagnoses were included in the selection phase. Despite the rigorous search process, it is possible that some studies might have been overlooked. Emotion-based stimulation is often related to psychosocial factors and requires other specific coordination; therefore, the current assessment range excluded studies focused on psychosocial emotional stimulation. As therapists and environmental factors often play important roles in patient recovery rates during the rehabilitation process, our review sought detailed information on emotion-based stimulation that was applied during training as a therapeutic intervention for the rehabilitation of stroke patients because the improvement of a patient’s motivation and emotional state can serve as an effective therapeutic method in a rehabilitation environment. A therapeutic environment that provides sensory-based stimulation is an example of emotion-based stimulation applied to training content during rehabilitation.
Current research on emotion-based stimulation has often focused on visual and auditory methods. The findings show that emotional (positive/negative) stimulation has a significant effect on treatment for unilateral neglect and the recovery of cognitive abilities. In emotion-based stimulation, positive stimuli were more effective treatments than negative stimuli. Basal ganglia are known to interact closely with the frontal cortex. When damaged, they can cause cognitive and motor control impairments similar to those of the frontal cortex (Leisman, Braun-Benjamin & Melillo, 2014; Leisman & Melillo, 2013; Leisman, Melillo & Carrick, 2013). In other words, the basal nuclei are involved in the selection and activation of various cognitive, performance, or emotional programs stored in different cortical regions. In particular, the basal nuclei are involved in certain types of learning and contribute to motor learning through implicit memory tasks and repetitive attempts. This suggests that the cognitive loop processing of the basal nuclei is somehow involved in the ability to unknowingly learn the predicted results associated with a specific stimulus (Leisman, 2013; Leisman & Melillo, 2012; Melillo, 2011). In a previous study, Ripp (Ripp et al., 2018) revealed the strong connections between vision and auditory stimulation. One was the connection between the insula and the right putamen. In previous studies of similar implementations of multisensory stimulation, the right insula and putamen were involved. As a result, it is safe to conclude that the insula connected to the right putamen is part of a dedicated network for audiovisual multisensory stimulation (Li et al., 2015; Royet, Delon-Martin & Plailly, 2013). The study also emphasized that the stimulation of both hemispheres could be more effective than unilateral methods (Royet, Delon-Martin & Plailly, 2013; Yu, Li & Sun, 2016). Interestingly, none of the papers compared the difference between single and multisensory stimulation or the differences between stimuli types. Future studies should carefully examine the difference between the effects of multisensory stimuli and the effects of a single stimulus. Relatively few studies suggested olfactory stimulation or explained the effectiveness of upper extremity and balance ability. Olfactory information may indeed to contain both the “olfactory” representation of an object and the motor representation (Yu, Li & Sun, 2016). That is, the significant association between olfactory stimulation and activities, such as eating food, could lead to strong neurophysiological movement mechanisms (strong motor-evoked potential) in humans. As a result, the neutral or negative emotion-based stimulation applied to a patient could not significantly influence the kinematics compared to the positive stimulus (Kvickström et al., 2011; Tavor et al., 2014). Also, further consideration of factors based on the subject’s memory in the form of stimulation could have stronger synergistic effects on emotion-based stimulation for stroke patients. These factors can also affect the therapeutic environment developed for the client during treatment. We generally only describe the treatment environment in terms of access to space and comfort, and we are often unaware that emotion-based stimulation environments can also serve as treatment. Related literature describes strategies that can be used to implement changes to therapeutic training situations (Jesus & Silva, 2016; Stans, Dalemans, de Witte, Smeets & Beurskens, 2017). Improving the overall awareness of rehabilitation specialists to the potential impact of non-verbal and linguistic cues as well as other therapeutic environmental factors on the therapeutic situation is recommended. O’Halloran et al. (O’Halloran, Grohn & Worrall, 2012) insisted that experts should have comprehensive knowledge of the interventions required to adjust the physical environment to improve interactions with patients.
Some studies provided information and therapeutic recommendations for left and right hemisphere effects. Their findings showed the therapeutic dissimilarities of each hemisphere through variable activation of the brain hemispheres according to the application of emotion-based stimulation. According to interhemispheric inhibition, the left hemisphere (LH) is biased to handle positive emotions and the right hemisphere (RH) is biased to handle negative emotions. As a result, LH lesions should enhance the response to negative stimulation of RH, whereas RH lesions should enhance the response to positive stimulation of LH (Killgore & Yurgelun-Todd, 2007; Lovseth & Atchley, 2010). Buratto’s study (Buratto, et al., 2014) also found similar levels of false memory in both the RBD and LBD groups for negative photography; however, RBD patients showed greater reductions in false memory than LBD patients in the case of positive photographs. One study of patients with brain injuries revealed that the right hemisphere regulates emotion perception (Oren, Soroker & Deouell, 2013). Participants with damage to the right brain were found to be less accurate when trying to distinguish emotional aspects compared to either patients with left brain damage or healthy participants. In Grabowska’s study (Grabowska et al., 2011), the analysis of fMRI data showed that accurate detection of emotional stimuli on the left (injured) side was associated with higher activation of the limbic system (front cingulate), frontal cortex (FEF), and associated visual regions (post-genital gyrus). Conversely, it is notable that the correct detection of emotional stimuli on the right (damaged) side resulted in higher activation as the higher limbic system (front clavicle, insulator, and posterior cingulate) was combined with visual areas 18 and 19. This review also confirmed the therapeutic efficacy of the right hemisphere in stroke patients, and it confirmed that more therapeutic possibilities were generated from relatively positive emotional stimulation.
For the determination of clinical significance and future research, rehabilitation professionals should have a profound understanding of the requirements related to the provision of emotion-based stimulation of treatment content during the rehabilitation of stroke patients. However, experts must often work in inappropriate environments and are unable or incapable of modifying them. They require support from governing institutions and health care systems when attempting to adapt therapeutic environments. As can be seen from the results of this review, the application of emotion-based stimulation during treatment may contribute to improvements in therapeutic effectiveness that can ultimately benefit stroke patients. In particular, emotion-based stimulation can now confirm the therapeutically effective impact on patients with right hemisphere lesions. The results of this review show that rehabilitation therapists require more experience and awareness of certain factors during training. Emotion-based stimulation requires careful attention when adjusting the three types of therapeutic effects and the treatment environments based on them. Most of the reviewed articles described studies of specific phenomena, and there is still a dearth of research on the effects of emotion-based stimulation on stroke patients. In order to better understand the impact of training conditions and environments on stroke patients and provide strategies for improving treatment conditions, further studies must be conducted. In addition, qualitative research methods can be used to evaluate user satisfaction among the methods that best demonstrate therapeutic effectiveness. Therapeutic effects according to types of stimuli can be identified, and the differences among application methods can be studied using quantitative methods. Brain studies that can identify therapeutic dissimilarities according to right and left hemisphere lesions may clarify the potential effectiveness of treatment.
Conclusions
This review found that strategies for adjusting emotion-based stimulation environments for the therapeutic rehabilitation of stroke patients (e.g., using visual, auditory, and olfactory stimuli) can positively affect the functional recovery of patients. Adjustments to emotion-based stimuli can help persons with unilateral neglect and cognitive impairment respond better and receive positive training feedback, thereby leading to more effective rehabilitation. Specialists in the field are encouraged to have a broad understanding of therapeutic situations and their potential impact on environments. As expressed in this review, insufficient attention has been given to the differences between the pros, cons, and effectiveness of each type of sensory stimulation.
Conflict of interest
None to report.
