Executive dysfunctions mediate between altered sensory processing and daily activity performance in older adults

Sensory processing refers to the way individuals manage incoming sensory information, including its reception, modulation and integration with other brain areas and networks, to produce an adaptive output to environmental demands [1]. Since sensory systems provide the brain with ongoing information about the environment, adequate sensory processing is fundamental for proper cognitive and emotional function, for accurate movements, for learning, for socializing and for other activities that characterize our daily lives [2].

Altered sensory processing refers to difficulties to modulate and organize the intensity of response to sensory input in a graded and adaptive manner. Altered sensory modulation result in hypo or hypersensitivity to sensory input. Individuals with hypersensitivity respond to sensation faster, intensely and for a longer duration. They are overwhelmed with sensation and even experience “regular” stimuli as painful. This may lead to behavioral dysregulation expressed in stressful behavior, anxiety, irritability and avoidance from interactions with the physical and the social environments [1]. On the contrary, individuals with hyposensitivity tend to miss sensory stimuli and thus fail to respond accurately to environmental demands [1]. Both hyper or hypo sensitivity may restrict adaptive behavior [2] and interfere with daily activity performance [3].

One of the theoretical models that refers to the interaction between the neurological-threshold to sensory input and the related behavioral regulation is Dunn’s model [4]. According to this model, the interaction between the neurological threshold and behavioral regulation results in four patterns: (1) Low registration - people with high neurological thresholds (hyposensitive) and passive behavioral strategies that fail to detect sensory information and do not seek for it; (2) Sensory seekers - people with high neurological threshold who actively seek for rich and intense sensory stimuli (3) Sensory sensitivity – people with low neurological thresholds (hypersensitive) and passive behavioral, meaning they do not actively eliminate uncomfortable sensations; thus, they frequently experience discomfort, distraction, and emotional burden (4) Sensory avoiding - people with low neurological thresholds who actively limit their exposure to unpleasant sensations.

The very few studies that used Dunn’s model in older people, found that older people tend to show lower registration of sensory input, lower tendency to seek for sensory input and in some cases have modulation difficulties that result in hyper sensitivity. These alterations were found to significantly interfere with daily activity performance, with participation in daily situations and reduce quality of life [5, 6].

Nevertheless, most studies about sensory processing and modulation in the elderly focus on sensory acuity or sensory impairment in a specific sensory modality, mainly visual, auditory and vestibular [7‐11], as measured in laboratory settings. Less is known about the ability of elderly people to process and modulate sensory information from various modalities, in daily life scenarios [5]. Moreover, the literature emphasizes that the aging brain tends to rely increasingly on multisensory integration rather than on a unisensory modality to compensate for the neural and sensory deterioration [12]. Hence, studies should further explore alterations in sensory processing and modulation in older adults, as expressed in all modalities and in daily life scenarios, in order to create better intervention programs, that are not relevant only for the clinical setting, but may be applicable to daily environments. For that, studies should also elucidate the contribution of relevant factors responsible for behavioral regulation that affect the adaptive responses to environmental demands, such as the high cognitive abilities named executive functions (EFs) [13‐15].

The high cognitive abilities responsible for behavioral regulation, for formulating goals, planning how to achieve them, and carrying them out effectively [16] named EFs, are extremely affected by aging and significantly interfere with daily activity performance [17]. Decline in EFs in older adults, as a result from neurodegenerative changes [18] is related to deficient performance of instrumental activities of daily living (IADL), and impairment in elementary activities that enable keeping daily routines, such as: driving, money management, shopping [19‐21]. The evaluation of EFs in the elderly is also challenging – in most cases EFs are measured by laboratory neuropsychological/cognitive measures, which mainly focus on specific aspects of EFs such as inhibition; shifting, etc. with no referral to the implications on people’s daily function [22, 23]. In order to better reflect the implications of EFs on daily activities, ecological valid assessments that imitate daily scenarios are needed [24‐26]. One of the efficient ecological valid assessment which evaluates the multicomponent expressions of the EFs in daily life scenarios is the Behavior Rating Inventory of Executive Function–Adult version (BRIEF-A) [27].

Yet, very few studies refer to the association between sensory processing and EFs. The existing data collected on populations with central nervous system abnormalities such ADHD, brain injuries and stroke, found that altered sensory processing was related to reduced EFs expressed for example in attentional problems, impaired working memory and inhibition problems [28‐31].

Although studies show that altered sensory processing in the elderly affects daily activity performance, and may be related to executive dysfunctions, less is known about the contribution of EFs to the impacts of altered sensory processing on daily activities. Understanding how the ability to regulate behavior, manage actions and decisions modulates the connection between altered sensory processing and daily activity performance is critical for intervention programs. By understanding the role of sensory processing, EFs and the relationships between them, in determining functional resilience or vulnerability, prevention and intervention programs may improve daily function and quality of life in the elderly. Based on the above, this study aimed to profile altered sensory processing in older adults, in all sensory modalities, as expressed in their daily life and to explore whether EFs mediate the relationship between sensory processing and the individual’s ability to perform daily activities. It was hypothesized that EFs indeed mediate the relationship between sensory processing and daily activity performance.

To understand the participants’ characteristics better, we first describe their sensory processing abilities, EF, and cognitive deficits in daily activities, as measured by the AASP, BRIEF, and DLQ, respectively.

This study focused on altered sensory processing, executive dysfunctions and their impacts on daily activity performance in older adults. The main findings are that (a) older adults have less efficient sensory processing and reduced EFs, as expressed in their daily life scenarios (b) EFs mediate the relation between altered sensory processing and daily activity performance. This means that, even if sensory processing is altered in older adults, it is the better or worse EFs that define their level of impact on daily activity performance.

When referring to the specific sensory processing profiles - most participants scored within the normal range of each AASP sensory profile. Since this study’s sample included relatively healthy and functional older adults, the sample appears representative of sensory processing in the older population. However, when examining the prevalence of participants with extreme sensory processing, according to the AASP, 9% had difficulties registering sensory input and about 25% had lower tendency to seek for sensory input. Indeed, older adults may require a greater amount of sensory input to react. If this amount is not provided, it may lead to lower awareness of the environment [39, 40, 41]. A similar prevalence of above- and below-AASP norms was noted in sensory patterns with low neurological thresholds (sensory sensitivity and avoidance), highlighting the modulation difficulties.

Whether sensory input from the daily environment is experienced as overwhelming, or, on the contrary, is missed because of hyposensitivity, other abilities - physical, cognitive, and emotional - may decline [42‐44]. Thus, the individual’s interaction with the environment may be impaired and restrict the engagement in daily occupations and activities. These functional limitations may contribute to social withdrawal [1] and isolation [45] known to be prevalent in the elderly and severely reduce quality of life and well-being [46]. Thus, prevention programs should screen for sensory-processing alterations in older adults and understand their implications on daily life and on the persons’ well-being.

The second significant outcome of this study emphasizes that referring only to sensory processing is insufficient. Science and practice should also consider other key factors that may affect the interactions between the individual and his/her physical and social environments. In this study, the assumption was that hyper or hypo sensitivity to sensory input does not stand alone as a factor that influences the interaction with the environments and the performance of daily activities. As mentioned in Dunn’s model [4], it is the interaction with the person’s ability to regulate his/her behavioral response to the sensory input, that contributes to activity performance. Indeed, in this study, the high cognitive abilities named EFs, that are responsible for an individual’s-controlled goal-oriented behavior mediated between sensory processing and daily activity performance. Executive dysfunctions, as expressed in daily life situations, were found in about one-third of the sample. This result highlights several points: first, the vulnerability for executive dysfunctions warrants attention also among “normal” older adults. Second, due to the EFs domain’s complexity, it is not enough to evaluate separate EFs components in the lab. A transition to real- life context is necessary. For that, appropriate performance-based measures should be used to evaluate EFs expressions and functional impacts in the real world [47]. Evaluations such as the BRIEF-A and DLQ provide clinicians with practical functional knowledge that bridges clinical observations with people’s function in their natural environments. Third, the analysis of the SEM model showed that altered sensory processing was associated with reduced EFs as reflected in behavioral regulation and in meta-cognition measured by the BRIEF, supporting the study hypothesis. Neuro-imaging findings explain this association by referring to the connection between the prefrontal cortex (which plays a central role in EFs), the sensory cortical areas and the thalamic reticular subnetworks [30, 48, 49]. However, additional implications should be derived. First, the SEM model highlights the role of different facets of each of the EFs domains. For example, the interaction between AASP and BRIEF-A scores was most emphasized in sensory patterns related to passive strategies in Dunns’ model (low registration and sensory sensitivity). Moreover, low registration and sensory sensitivity had significant indirect effect on DLQ, mediated by the BRIEF-A. This may suggest that people who use passive strategies to deal with sensory input are more vulnerable and have less efficient coping mechanisms, which in turn, restrict their daily activity performance. On the other hand, individuals who seek for sensory input and enjoy it in their daily life, experience better well-being and quality of life [50]. This point should be examined in further studies.

Prevention and intervention programs for older adults should refer to both sensory processing and EFs [51]. Given that sensory-processing alterations worsen with age, earlier screening is a significant preventive aid. The relationships between altered sensory processing and EFs (meta-cognition and behavioral regulation) and their influence on daily activity performance should receive growing attention in clinical programs for older adults. For that, assessments with ecological validity that reflect how age-related dysfunction are expressed in people’s real lives and affect daily performance are most relevant. These assessments may elevate the individuals’ awareness to their dysfunctions. Individuals may better notice when and how their dysfunctions interfere with daily activity performance. With this knowledge, clinicians may suggest strategies to deal with difficulties related to altered sensory processing and EFs, and overcome obstacles in daily activity performance [52]. These strategies promise better intervention outcomes in terms of enhanced participation in daily settings and better quality of life, which are the main measures of intervention efficiency according to the World Health Organization [53].

Altered sensory processing and executive dysfunctions may be prevalent in older adults. Among older adults with altered sensory processing, better or worse EFs may define the level of daily activity performance. Thus, evaluations of sensory processing should be proceeded in measuring EFs. By using measures with ecological validity, clinicians may better understand the expressions and impacts of altered sensory processing and executive dysfunctions on people’s daily life. This information may be useful for focusing intervention goals and strategies based on the individual’s specific profiles and needs in real life context.