Heavy usage was found to be associated with impaired attention, reduced numerical processing capacity, changes in social cognition, and reduced right prefrontal cortex (rPFC) excitability. Memory impairments were not detected. Novel usage over short period induced a significant reduction in numerical processing capacity and changes in social cognition.

Heavy users showed increased impulsivity, hyperactivity and negative social concern. We also found reduced early TMS evoked potentials in the rPFC of this group, which correlated with severity of self-reported inattention problems. Heavy users also obtained lower accuracy rates than nonusers in a numerical processing. Critically, the second part of the experiment revealed that both the numerical processing and social cognition domains are causally linked to smartphone usage.

Subjects lacking previous experience with smartphones (n = 35) were compared to a matched group of heavy smartphone users (n = 16) on numerous behavioral and electrophysiological measures recorded using electroencephalogram (EEG) combined with transcranial magnetic stimulation (TMS) over the right prefrontal cortex (rPFC). In a second longitudinal intervention, a randomly selected sample of the original non-users received smartphones for 3 months while the others served as controls. All measurements were repeated following this intervention.

Funding: The author received specific funding for this work from the Israeli Ministry of Science under the Prat and Eshkol scholarships. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2017 Hadar et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

Many human functions are now supported and mediated by smartphone devices. It has been argued that usage comes with a price: it has been associated with an increasing accident rate, sleep disorders, undesirable mental health outcomes and persistent changes in behavior and personality [1,2]. Indeed, the potential negative impact of smartphone on human behavior has not completely escaped the eyes of policy makers. For instance, authorities began imposing heavy penalties on drivers and even on pedestrians using smartphones [3–5].

Given the sheer frequency and duration of daily smartphone usage it is conceivable that changes in cognition, behavior and psychological states may be observed in users. Such changes have been found in intensive users who present an exaggerated and debilitating usage [6,7]. Recent studies showed an association between such usage and impulsive behaviors [8], pathological dependence [9], low emotional stability and self-esteem [10], chronic stress [11], depression [12,13], and sleep disturbances [2,11]. A larger study of 5051 adolescences, found that heavy users were significantly more likely to attempt suicide as compared with normal users [12]. However, these recent studies offer primarily questionnaires-based correlative data and thus little can be inferred in terms of causal changes to cognition and behavior.

Some researchers conceptualized behavioral changes associated with smartphones and similar technologies as a behavioral addiction [14–16]. Kown et al. (2013) generated and validated the Smartphone Addiction Scale (SAS), based on previous internet addiction diagnostics, and several similar scales have been developed [17]. However, despite the upsurge in diagnostic instruments, to date there is no evidence demonstrating that smartphones alter objectively measured behavior [18]. In order to bridge this gap in the literature this multifaceted study sought to explore smartphone associated changes on 3 planes: 1) self-reported and objective records of behavioral tendencies, 2) behavioral task performance, and 3) recording of a relevant neural circuitry.

The first was addressed by using series of questionnaires assessing traits and behavioral tendencies that characterize problematic use of mobile phones and internet (11,12,16). Specifically, psychosocial disorders, depressive symptoms, and loss of impulse control emerged from the literature as dominant in such users [19–21]. For instance, internet usage has been shown to increase impulsivity in heavy users, and similar results were obtained in computer gaming addiction [21]. We thus predicted that heavy smartphone users will present with abnormal scores of social cognitions, depression, and ADHD measures. To account for the versatile nature of self-report data we also monitored actual smartphone usage using a smartphone software. We sought to assess whether objectively measured usage will be proportionally linked to severity of reported symptoms.

The second was addressed by employing tasks assessing impulsivity, attention in information processing and memory. The selection of these domains stemmed from the current knowledge in the fields on internet addiction disorder (IAD). The most consistent behavioural finding in these disorders is poor inhibitory control suggesting greater impulsivity [22,23]. Equally important, several studies suggested an association of attention grabbing stimuli with memory and attention deficits [24–26]. In addition, numerous studies implicated digital addictions (internet and gaming) in more generalized executive control dysfunctions [27,28]. Executive control processes such as working memory performance and decision making were reported to be particularly reduced in the presence of digital devices. We thus selected a classic response inhibition task [29], a speeded and difficult numerical information processing task, and a recognition task. We speculated that given the overarching dependence of smartphone users on the devices for simple calculations and as a memory aid, they may exhibit impaired capacity for technologically unassisted information processing and retention of information.

The third plane, relevant neural activity, was addressed by measuring right prefrontal cortex (rPFC) excitability previously implicated in impulse inhibition [30]. Internet and gaming addiction, currently defined as impulse control disorder [24], have both been associated with abnormal prefrontal activity at rest [24]. In a recent review by Weinstein and colleagues the neural mechanisms underlying internet and gaming addiction have been suggested to closely resemble the neuropathology of substance addiction [31]. Reduced gray and white matter volume have been repeatedly found in the prefrontal cortex, the orbitofrontal cortex and the supplementary motor area of subjects with internet and gaming addiction; changes that correlated with the duration of the disorder [24] [31]. We thus measured right prefrontal activity to establish whether sensitive neuronal changes occur in association with heavy smartphone usage. For this purpose, we measured several indices of rPFC excitability. First, early transcranial magnetic stimulation (TMS) evoked potential (TEP) was used to compare glutamatergic-related [32] cortical excitability at rest. Second, long interval cortical inhibiton (LICI) was used to evaluate a correlate of gama-aminobutyric acid (GABAb)- mediated activity of inhibitory interneurons [33,34].

Finally, we sought to determine whether smartphone usage can autonomously cause such changes. For this purpose we employed an additional longitudinal randomized controlled design in which a sample of nonusers received a smartphone while a matched control sample remained with their original mobile phone (Fig 1); a design that serves two aims. First, it allows identification of cognitive, behavioral and neuronal alterations in heavy smartphone users, by comparing the results of the two populations (heavy- vs. non-users). Second, it allows to determine whether usage produces measurable behavioral and neural changes.