Edited by: P. Hemachandra Reddy, Texas Tech University, USA
Reviewed by: Ramesh Kandimalla, Texas Tech University, USA; Hisao Nishijo, University of Toyama, Japan
*Correspondence: Maria Clotilde H. Tavares, Laboratory of Neurosciences and Behavior, Department of Physiological Sciences, University of Brasilia, Brasilia, 70910-900, Brazil
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A new tablet device version (IOS platform) of the Spatial Delayed Recognition Span Task (SDRST) was developed with the aim of investigating visuospatial Working Memory (WM) abilities based on touchscreen technology. This new WM testing application will be available to download for free in Apple Store app (“SDRST app”). In order to verify the feasibility of this computer-based task, we conducted three experiments with different manipulations and groups of participants. We were interested in investigating if (1) the SDRST is sensitive enough to tap into cognitive differences brought by aging and dementia; (2) different experimental manipulations work successfully; (3) cortical brain activations seen in other WM tasks are also demonstrated here; and (4) non-human primates are able to answer the task. Performance (scores and response time) was better for young than older adults and higher for the latter when compared to Alzheimer’s disease (AD) patients. All groups performed better with facial stimuli than with images of scenes and with emotional than with neutral stimuli. Electrophysiology data showed activation on prefrontal and frontal areas of scalp, theta band activity on the midline area, and gamma activity in left temporal area. There are all scalp regions known to be related to attention and WM. Besides those data, our sample of adult captive capuchin monkeys (
Memory involves the ability to acquire, retain and utilize information and knowledge. This fundamental process allows learning and adaptive behavior, considering that the organism can use its previous experiences to select the most appropriate behavior for the upcoming situation (Simon and Kaplan,
The conception of WM grew up of the literature on short-term memory (STM) in the mid 1970s (Baddeley and Hitch,
In 1887, Joseph Jacobs, researching on STM, introduced the so-called digit span to measure the capacity of STM. The task consisted of presentation of a random series of digits which participants had to repeat in their correct serial order. The longest sequence correctly repeated was comprized by approximately 6 or 7 items. That figure was understood as the capacity of STM. This limited capacity to remembering some information (named “chunk capacity limits”), was later reported by Miller (
In a more recent development of his model, Baddeley describes four main components of WM: a control system of limited attentional capacity called the central executive; the episodic buffer, responsible for the association of new and old information; and two subsidiary storage systems, named the phonological loop—holds and manipulates speech-based information, and the visuospatial sketchpad (VSSP) performs a similar function for visual and spatial information (Baddeley,
In neuropsychology, there is abundant evidence linking the dorsolateral areas of the prefrontal cortex (DLPFC) to a range of executive processes, including the processing and maintenance of spatial stimuli in WM (Rudkin et al.,
In most studies, WM is accessed using different types of neuropsychological tests, including standard pencil-and-paper tests and computerized tasks with different methods and apparatus. Particularly the concept of specialized visuospatial component has received a growing amount of attention over the last decades (Logie,
Until today, span measures remain the gold standard for estimating WM capacity (Conway et al.,
The distinction between visual information (appearance) and spatial information (where the object are located) is a critical dimension in visuospatial WM. In this line, numerous modified versions of the spatial span task have been described in the attempt to develop a more sensitive paradigm for measuring visuospatial WM. However, one of the limitations of those tasks is the difficulty in applying them to general or clinical populations, such as older adults and Alzheimer’s disease (AD) patients, or in making a bedside evaluation. They are also difficult to being equally used by humans and non-human primates.
The “Spatial Delayed Recognition Span Task” (SDRST) have been used in an attempt to assess memory function within spatial and nonspatial domains. It has also been used to test memory capacity in aging or following a variety of neurologic disorders in non-human primates and humans. In general, the task requires the ability to identify a novel stimulus among an increasing array of previously presented stimuli using either spatial or nonspatial cues. Because participants have to hold spatial locations “online” and update them constantly to adjust to new information while answering the task, the SDRST is indeed tapping into visuospatial WM abilities (Lacreuse et al.,
Therefore, using that paradigm as reference, we devised a new computer-based task to evaluate visuospatial WM abilities, specifically WM load. This cognitive tool can be run on a tablet device (IOS platform) and would be sensitive to cognitive differences brought by aging and neuropsychiatric disorders. It can also be used in non-human primate studies.
The use of mobile devices, such as tablets, for this type of testing has several benefits. First, the test is run on a tablet computer with touch screen technology. This feature could be very promising especially for older adults, considering that many of them are less familiar with computers. Second, computerized tests include better standardization in administration, precise stimulus control and scoring without manual operation. They record performance and reaction time accurately and can generate a mass of seemingly precise data developing large and accurate databases. Third, this new version of the task also permits the manipulation of experimental parameters such as presentation time, shape, type and other characteristics of stimuli, which generates numerous alternative forms suitable for repeated testing. Fourth, the SDRST application is available for free in Apple Store app (“SDRST app”), so the test can be taken at no-cost. Finally, it is important to note that the use of computerized cognitive tasks on portable devices allows assessments to be made in a wide range of environments. This task can be used, for instance, in the context of everyday life, schools, hospitals, laboratories, universities, and research institutions. Practitioners may also carry out tests when visiting patients.
In the current paper we discuss the format of the new task and its advantages by presenting data that evidences its successful use with different populations and types of stimuli.
This test was developed by our group and runs in Delphi programming language for desktop using the computational program SYSMEN. It was presented in a touch screen monitor (LG Studio Works 440, Microtouch 17’) within arm’s reach distance. Additionally, this module was adapted in Objective C language, compatible with mobile devices on Apple/iOS platform.
In this task, participants are required to discriminate a novel location of a stimulus among an increasing array of stimuli presented sequentially in various locations on the screen. A stimulus is presented in one of the possible locations on the screen and the participant has to touch it and reappears at the same location along with a second stimulus in a different location. The participant has to touch the stimulus that is in this new location, which will make both disappear and reappear at the same locations along with a third stimulus in a new location. These steps continue for the maximum number of stimuli pre-selected by the experimenter or until a mistake is made (Figure
It is worth mentioning that the tool can be used in a wide variety of settings. The examiner can select the best configurations for the study: stimulus characteristics (colors, shapes, emotional valence, contextual images, faces, etc.), the size of the stimuli, the background color, the time of exposure of the stimuli on the screen, how many different stimuli will be used on the same trial and in the total of trials, how many trials and which stimuli will be used, how many stimuli will compose one trial, the interval time between two stimuli appearance, the distance between the screen and subjects, amongst others. Additionally, the examiner can determine whether the same stimulus will be shown repeatedly on the same trial or select different stimuli (Figure
For research studies we suggest, when using the tablet, the device to be placed over a table or other hard surface that raises the height of the tablet. This will reduce motion artefacts, such as head movements and also remove muscle stress from the body. Nevertheless, one of the useful features of the SDRST is the flexibility with which test parameters can be chosen. Thus, we consider that examiners may place the tablet in the most appropriate way for their studies, taking into account the type and size of stimuli, as well as their objectives.
The computer software registers demographic information of the participants (Figure
Three sets of studies were conducted using the SDRST, with a total of 172 participants. All participants were right-handed according to the Edinburgh Inventory (Oldfield,
Study “a” (Satler and Tomaz,
Study “b” (Belham et al.,
Study “c” (Garcia,
Demographic details are shown in Table
Characteristic | YA | OA | AD |
---|---|---|---|
N | 84 | 64 | 22 |
Age, years | 21.23 (2.63) | 70.45 (6.55) | 78.27 (6.70) |
Sex (M/F) | 43/41 | 30/34 | 7/15 |
Education, years | 13.44 (1.49) | 13.59 (5.12) | 6.73 (4.00) |
Both YA and OA were screened for cognitive impairment with the Mini-Mental State Examination—MMSE (Folstein et al.,
Participants had to discriminate a novel location of a stimulus among an increasing array of stimuli presented sequentially in various locations on the screen. A stimulus was presented in one of the 16 possible locations on the screen and the participant had to touch it and the reappears at the same location along with a second stimulus in a different location. The number of stimuli would increase up to a maximum of 8 stimuli within one trial. All the stimuli were colored images sized 4 cm × 4 cm.
Study “a” and “c” used geometric pictures and IAPS images (Lang et al.,
Study “b” used geometrical images and facial photographs representing negative, positive and neutral expressions. Each participant completed 10 trials with each emotional valence. The interval time between stimuli was 3 s. Correct answers led to an acute auditory feedback signal, and wrong answers, to a bass auditory signal.
Participants were received in the experimental room, where they read and signed the written informed consent. After that, they were invited to sit comfortably in front of the touch screen, which was positioned within the reach of the volunteer, and to answer the neuropsychological tests. Then, the instructions for the SDRST were read and participants answered one training session to verify if the test rules had been understood. Instructions were kept constant for all subjects. The time of execution of the task varied according to each participant’s response time, but the full procedure did not last more than 2 h. All participants used their dominant hand to perform the task.
Several analyses were conducted in order to evaluate the feasibility of SDRST to tap into WM in different experimental conditions and with different groups of participants. Performance on the task was measured by the mean of corrected responses before a mistake in each trial. On the next sessions, we provide a brief description of the performance of participants (YA, OA and AD patients) using geometric, complex figures (International Affective Pictures System—IAPS, Lang et al.,
Types of stimuli | Task condition | Emotional valencea | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
IAPS | Faces | Unique | Varied | Negative | Positive | Neutral | ||||||||
M | SD | M | SD | M | SD | M | SD | M | SD | M | SD | M | SD | |
YA | 7.11 | 0.75 | 7.19 | 0.46 | 7.15 | 0.67 | 7.36 | 0.99 | 7.56 | 0.44 | 7.27 | 0.71 | 7.42 | 0.70 |
OA | 4.96 | 1.57 | 5.96 | 0.94 | 5.35 | 1.42 | 6.41 | 1.34 | 6.16 | 1.06 | 5.85 | 1.02 | 5.90 | 1.22 |
AD | - | - | 4.09 | 1.56 | 4.62 | 1.80 | - | - | - |
Study “b” utilized geometrical pictures and emotional facial expressions as stimuli in a total of 40 trials (Belham et al.,
Study “a” examined the WM performance in mild AD patients and healthy elderly controls, assessed with the SDRST (Satler and Tomaz,
On these analyses, we tested how participants’ performance would differ if we presented the task in distinct conditions: unique and varied. In the first one, all stimuli presented in the same trial were identical and only differ from trial to trial, whereas in the varied condition, stimuli were always different.
For these analyses, data of studies “a” and “c” were used. Analysis of Variance (ANOVA) showed that there was a main effect of the condition for YA (
These results indicate that, when shown different stimuli on the same trial, participants have an extra mnemonic element to help responding the task. The variation on the content of the stimuli leads to a more active participation of the episodic buffer besides the regular visuospatial sketchpad activation. It also suggests that this happens regardless of the age or the psychological condition of the participant.
For this analysis, we were interested in investigating what would happen with young and older adults’ performance if we used two different types of stimuli: faces and scenes. Data from the three studies were analyzed. The faces were chosen based on a pilot study done with young and older adults and depicted adult models manipulated to only show the face with no interference from hair or other body parts. The scenes were selected from the IAPS, which is a set of static images containing various pictures depicting snakes, mutilations, accidents, illness, puppies, babies, and landscapes, among others (Lang et al.,
Results indicate that there was a main effect of the type of stimuli (
We used data from study “b” to investigate the influence of different emotional valences into WM during the SDRST. The facial images depicted anger, happiness or neutral expressions.
Data showed that negative images elicited a higher performance than positive images (
The SDRST has also been successfully used with non-humans primates (Belham et al.,
Studies “b” and “c” also measured the cortical brain activity of participants while responding to the SDRST. Electroencephalographic (EEG) data were recorded from 21 scalp channels following the 10–20 international system, plus two reference electrodes on the mastoids. Continuum records were made with a NeuroSpectrum 4EP system (Neurosoft, Russia) with impedances kept below 5 kΩ and a 2000 Hz sampling rate. Data were then processed with EEGLAB v.9.0.4.5 (Delorme and Makeig,
Data analysis showed cortical activation compatible with what is known for WM and spatial information studies. There was a greater activation in prefrontal and frontal areas of scalp, which is consistent with the type of activity seen for WM tasks (Speck et al.,
The present paper describes a new computer-based task to evaluate visuospatial WM abilities, in which participants are required to maintain the spatial information of a crescent sequence of items online and make decisions about them. We show that this version of the Spatial Delayed Recognition Memory Task is sensitive to the natural age-related cognitive differences and also to the deficits brought by AD. We also present data indicating that the manipulation of type, complexity, variability and emotional valence of stimuli is possible and successful in studies about WM load. The fact that capuchin monkeys were able to complete this task in a touch-screen monitor will allow future comparative studies between species. Electrophysiological findings corroborate that areas known to be related to executive functions, WM and decision making are activated during this task. Therefore, this new version of the SDRST seems to be a reliable and sensitive measure to investigate visuospatial WM in different groups of participants, including clinical and non-clinical populations. It may represent a useful and effective cognitive measure to detect cognitive changes associated with normal aging and dementia. From a public health point view, the new approach could help to collect large-scale data from aged people in general population in the world by connecting the system to the internet. Mobility and free cost of the application (SDRST app available to download for free in Apple Store app) are also benefits of the tablet device approach.
CS, FSB, AG, CT, MCHT conceptualized and designed the work. CS, FSB, AG acquihired and analysed the data. CS, FSB, AG, CT, MCHT interpreted the data. CS, FSB drafted the work. CS, FSB, AG, CT, MCHT critically revised and approved the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors would like to thank Joabe Alexandre Leite for adapting the new SDRST version for mobile devices.
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