Introduction

The varied combination of multimodal sensory stimuli present in environmental enrichment induces biochemical changes that enhance neural plasticity and neuroprotection¹. This allows an optimal adaptation of the central nervous system to the changing sensory demand of the environment through enhanced morphofunctional reorganization and synaptic consolidation, which optimizes sensory-motor and cognitive-behavioral learning². Therefore, an enriched environment allows generating a zone of well-being where the person interacts in an optimal and novel way with a variability of complex stimuli, generating greater experience-dependent neural plasticity versus traditional stimulation³.

The literature defines the environmental enrichment paradigm, from cognitive neuroscience, as a contextual combination of complex inanimate and social stimuli that facilitate sensory, motor, cognitive, and socioemotional skills⁴. This definition focuses on how contextual enrichment can optimize the adaptation and functioning of neural networks, validating it as a potential low-cost intervention model applicable to educational⁵, neurological⁶, and mental health⁷. The transversality of the intervention model is particularly interesting for patients with intellectual disabilities, who may see their performance affected in these three areas.

Intellectual disability is characterized by deficits in cognitive abilities and limitations in the ability to adapt to the environment and social environment⁸, originating before the age of 18 years⁹. Its etiology is varied, encompassing various diagnoses such as unspecified genetic syndromes, Down syndrome, neurodevelopmental disorders, and among others¹⁰. Environmental enrichment has been shown to be a viable intervention strategy in animal models of intellectual disability¹¹-¹³; however, evidence in human models is still incipiently developing¹⁴.

In recent years, there have been different review studies that directly or indirectly characterize the effects of environmental enrichment on intellectual disability. There are systematic reviews that highlight the effects of this paradigm on cognitive-behavioral and sensorimotor variables in neurological rehabilitation in adults¹⁵ and in animal models of acquired brain injury¹⁶. In turn, there have been narrative reviews on the reaches of environmental enrichment on age-dependent cognitive reserve in animal models¹⁷-¹⁹, on learning in the classroom²⁰ and in animal models in intellectual disability¹¹,¹³; however, to date, no systematic review focused on the neurocognitive effects of environmental enrichment in intellectual disability in children and adolescents has been identified.

Therefore, the aim of this article was to characterize the neurocognitive effects of protocolized environmental enrichment interventions in children and adolescents with intellectual disabilities. This will provide reliable and updated information that will allow incorporating the principles of this paradigm in the design of public policies and educational, social, and health interventions.

Method

An electronic and systematic search of articles was performed following the systematic review methodology based on the international PRISMA guidelines²¹, which was developed in two processes. The first aimed to identify the studies to be included and the second to elaborate a matrix with the purpose of extracting information from the studies for subsequent analysis. The article selection process involved five stages (identification, duplicate, screening, eligibility, and bias) which can be seen graphically in figure 1.

Figure 1 Flow diagram of the search and selection of articles in the study identification process. 

The identification stage consisted of searching for articles in the Web of Science (WoS), Scopus, EBSCOhost, and PubMed databases using the keywords “environmental enrichment,” “intellectual disability,” “children,” and “teens,” their synonyms, extensions, and conjugations, together with the use of Boolean OR and AND terms. A search iteration was performed and the filters specific to each database were applied in relation to the date of publication between January 2000 and October 2020, and type of document article (for syntax used by database, Supplementary Table 1). The final search was performed on October 3, 2020. The duplicate stage consisted of eliminating those studies that had a literal copy of the selected text. The screening stage consisted of a review by two independent judges, who were presented with a protocol to evaluate the objective of the review and the keywords to be identified in the title and abstract. Articles that did not contain the key words or did not respond to the objective of this review were eliminated. Articles were also eliminated when two judges considered that they should not be included. Discrepancies were resolved by a third reviewer who decided whether or not to include the article. The eligibility stage involved the downloading and complete reading of the research and the application of the previously established exclusion criteria. Quantitative empirical research that explicitly stated the use of environmental enrichment protocols²² in children and adolescents²³ with intellectual disabilities were included in the study. Exclusion criteria considered were as follows: (1) article not available; (2) case study; (3) language other than Spanish, English or Portuguese; (4) qualitative research; (5) adult research; (6) animal model research; (7) theoretical research; (8) does not specify environmental enrichment; and (9) no diagnosis associated with intellectual disability. The bias assessment stage consisted of the review of the entire process by two independent reviewers, considering the exclusion criteria presented. Finally, the process for the analysis of the information from the included studies²⁴-³⁰ involved the aspects described in tables 1 and 2.

Results

Of the 1064 articles identified in the literature search, 450 were eliminated as duplicates and 465 were excluded at the title and abstract review stage. Of the remaining 149 articles, 115 were excluded due to the following criteria: theoretical study (27), qualitative study (10), animal model study (47), and adult study (31). Thirty-four articles passed to the full-text evaluation stage, where bias evaluation methods were applied with three independent reviewers and the elaboration of a table of excluded articles and reasons for exclusions (Supplementary Table 2). Finally, seven articles were selected for data extraction and analysis of results, through the design of two matrices describing the characterization of neurocognitive effects (Table 3) and the characterization of environmental enrichment protocols (Table 4). The process of identification and eligibility of items described above is shown graphically in figure 1.

Of the selected studies, developed in European and American continent, five have an experimental design²⁴-²⁸ and two quasi-experimental²⁹,³⁰. We identified four free designed, that is, non-patented environmental enrichment protocols that respond to the characterization of a specific sample: Young Director Children's Animation Studio (YDCA)²⁴, Turkish Early Enrichment Project (TEEP)²⁶, Project TEAM²⁸, and Enriched Environment ABAB Design²⁹. In turn, three patented protocols were identified with standardized procedures, independent of sample characterization: Drums Alive Kids Beats (DAKB)²⁵, Feuerstein Instrumental Enrichment Basic Program (IE-Basic)²⁷, and Program for the Education and Enrichment of Relational Skills (PEERS)³⁰. The baseline diagnoses of intellectual disability addressed in the selected articles are subdivided into oligophrenia²⁴, unspecified intellectual disability²⁵,²⁹, cognitive deficit²⁶,³⁰, and neurodevelopmental disorder with cognitive compromise²⁷,²⁸. The age range of participants ranged from 3 to 20 years. The neurocognitive variables assessed focus on self-determination²⁸, self-efficacy²⁸, intellectual ability²⁶,²⁷, social cognition²⁵,²⁸,³⁰, speech coherence²⁴, motor skills²⁵, and behavioral regulation²⁵,²⁹.

The neurocognitive variables of self-determination, intellectual capacity, and motor skills demonstrated statistically significant improvements on intervention with environmental enrichment protocols compared to control groups without associated environmental enrichment²⁵-²⁷. Specifically, in intellectual ability, significant differences were evidenced in abstract reasoning and fluid intelligence²⁷, and better long-term academic performance²⁶. Social cognition evidenced statistically significant changes following the application of both free designed²⁸ and patented²⁵,³⁰ environmental enrichment protocols. In behavioral regulation, a significant decrease in aggressive, destructive, and disruptive behaviors was observed following exposure to free designed²⁹ and patented²⁵ environmental enrichment. Speech coherence clinically improved in the experimental group exposed to environmental enrichment compared to the control group without associated enrichment, mainly in the subvariables of correctness, expressiveness and clarity of speech, vocabulary enrichment, syntax, and intrinsic motivation²⁴. No clinically significant changes in self-efficacy were present in the selected studies²⁸.

In relation to the design and implementation of environmental enrichment protocols, both the provider profiles, the frequency of intervention and the duration of intervention per session and overall, present high heterogeneity. Providers include trained teachers²⁵,²⁶,³⁰, tutors and trained monitors without specifying profession²⁶,²⁸,²⁹, and interdisciplinary teams²⁴. Intervention frequencies varied between two sessions²⁵,²⁸,³⁰ and five sessions^{29 week}ly with a duration between 45 min²⁷,³⁰ and 120 min²⁸. The total duration of the protocols varied from 2 to 7 weeks in targeted interventions²⁵,²⁹,³⁰, to 1 to 2 years in long-term interventions²⁶,²⁷. Only three studies specified follow-up of participants between 2 and 6 weeks²⁸,³⁰ up to 19 years²⁶.

Discussion

The aim of this systematic review was to characterize the neurocognitive effects of protocolized environmental enrichment interventions in children and adolescents with intellectual disabilities. For such purposes, first, we must differentiate environmental enrichment as a neuroscientific paradigm from enriched therapy or intervention. Environmental enrichment, as proposed by Heidi Janssen, involves creating experiences in which participants can engage in social, cognitive, and sensorimotor activities simultaneously³¹. This allows for increased opportunities for practice and promotes active participation³². Environmental enrichment merges with activities of daily life and social participation specific to the user's everyday life³³, therefore, there are programs contextualized in specific educational, work, or leisure realities. In contrast, the enriched intervention involves the enhancement of a unique dimension, not necessarily fulfilling the simultaneity among the four dimensions proposed by the neuroscientific model. In the enriched intervention, the participant can be an active or passive agent, and the activity is not necessarily designed in a situational context attentive to the user's reality²².

The results of this research demonstrate positive effects of environmental enrichment on different neurocognitive dimensions compared to controls without enrichment in children and adolescents with intellectual disabilities, which is justified based on findings in the field of cognitive neuroscience and neurobiology. These disciplines have demonstrated that the environmental enrichment paradigm induces varied neural plasticity responses in the central nervous system in both animal and human models, ranging from functional cognitive enhancement to potentiation of synaptic plasticity, adult hippocampal neurogenesis, synaptogenesis, and modulation of gene expression³⁴,³⁵. The diversity of multimodal sensory inputs implicit in environmental enrichment induce epigenetic changes that enhance neural plasticity and neuroprotection through upregulation of glutamatergic and GABAergic tone, and upregulation of angioglioneurins such as BDNF, NGF, IGF-1, VEGF, and EPO³⁶.

The horizontal improvement of different neurocognitive variables through environmental enrichment protocols not only sustains an improvement in the cognitive functioning of children and adolescents with intellectual disabilities but, in turn, also provides them with tools based on the contextual practice of activities of daily living and social participation that facilitate their effective educational, labor, and social inclusion. In fact, social models of inclusion theoretically respond to the paradigm of environmental enrichment, as it implies the interaction of sensory, motor, cognitive, and socioemotional factors³⁷. The intrinsic contextualization of the paradigm to the situational reality of the participants encourages the development of neurocognitive dimensions applied to the context itself, which facilitates its extrapolation to the user's daily life.

The only neurocognitive variable that did not show positive changes was self-efficacy. Self-efficacy is defined as a person's belief in his or her ability to achieve certain actions, which will influence thoughts about him or herself³⁸. It is interesting to hypothesize why self-efficacy did not improve in adolescents with intellectual disabilities who participated in the Project Team protocol²⁸. The study suggests that the non-variation in self-efficacy responds to the characteristics of the assessment instrument used; however, let us recall that children and adolescents with intellectual disabilities make external attributions of their successes (“I did well just by luck”) and internal attributions of their failures (“I'm just slow”) mainly due to a history of failed experiences with the environment. This makes them internalize a negative self-image and develop lower self-efficacy³⁹, which in adolescence may be less susceptible to change.

In this study, it can be observed that the design and execution of the environmental enrichment protocols are irregular at the time of establishing providers, frequency and duration. The provider of environmental enrichment is not technically defined, since, strictly speaking, the multimodality of the model and the range of contextual applications imply the formation of inter- and transdisciplinary teams for its optimal design and execution. The disparity in the frequency and duration of the sessions unfortunately responds to the lack of consensus in the literature on the methodological design and dosage of environmental enrichment paradigms⁴⁰, which is still a matter of research.

This systematic review presents a number of methodological limitations, such as including only papers published in English, Spanish, and Portuguese. The varied etiology of intellectual disability also represents a limitation per se, as it increases the plurality of the sample of studies analyzed. In addition, the methodological design, the environmental enrichment protocols, and the neurocognitive variables evaluated are heterogeneous, respond to different situational contexts, and include the baseline bias of the instruments used to evaluate.

Conclusions

The application of environmental enrichment protocols in children and adolescents with intellectual disabilities has a positive impact on neurocognitive variables associated with intelligence, communication, socialization, and motor skills. The environmental enrichment paradigm is supported by scientific evidence in animal and human models. In turn, its guidelines encourage effective inclusion in activities of daily living and social participation of participants; however, it has methodological limitations that should be addressed in future research.

This systematic review is projected as a prelude to future research to better elucidate the benefits of environmental enrichment in intellectual disabilities. This will allow the foundation of base guidelines for public policies and programs of social, educational, labor, and health intervention that favor this profile of patients.

SUPPLEMENTARY DATA

Supplementary data are available at DOI: 10.24875/RMN.21000012. These data are provided by the corresponding author and published online for the benefit of the reader. The contents of supplementary data are the sole responsibility of the authors.