Every day we store and recall environmental information (e.g., writing down a phone number, making a mental shopping list, following the directions of a navigator along a route, and so on) and this storing and recalling activity relies on the working memory (WM): a multicomponent system that allows the integration and processing of a limited number of information for a short period of time (Baddeley and Hitch, 1974; Miller and Buschman, 2015). While working memory has limited capacities in terms of the amount of information that it can retain and its retention duration (Cowan, 2008, 2009; Cowan and Rouder, 2009), it allows for making calculations and solving tasks, and assists executive functions, including selective attention, reasoning, and planning (Cowan, 2014; Tang et al., 2019).

One of the components of the working memory is the visuospatial sketchpad (Baddeley and Hitch, 1974), described as the subsystem responsible for maintaining and processing visuospatial information. Accordingly, the visuospatial working memory consists of two separate subcomponents that encode, respectively, the perceptual characteristics of stimuli (shape and color) and their spatial position (Logie and Marchetti, 1991; Peterson, 2020). Different factors can influence how stimuli are encoded and stored in the visuospatial working memory; among these are salience, contextual information, stimulus quantity and position, binding, shape, and temporal duration (Emrich and Ferber, 2012; Pan and Luo, 2012; Souza and Oberauer, 2014; van Ede et al., 2017). In the present study, we will focus on the role attributed to the visuospatial working memory in processing temporal characteristics of the stimuli, which according to Mammarella et al. (Mammarella et al., 2013) requires an additional distinction for simultaneous and sequential presentation modality (Peterson, 2020). The first refers to spatial locations presented simultaneously in a working memory task and is related to static processes (Pickering et al., 2001), whereas the sequential modality refers to spatial locations sequentially presented so that individuals must recall each previous position. This is a dynamic process (Pickering et al., 2001). This distinction entails that the temporal characteristics of environmental stimuli are encoded and retained in the working memory to define a temporal continuum of events, to sequence the elements that are scattered along a path, to keep track of when a stimulus enters our perceptible space and then leaves it, to consider the temporal distance between one stimulus and another etc. Therefore, like other cognitive functions, working memory operates in a context in which time is an essential characteristic and this applies to visual, auditory, and tactile modalities (Wu et al., 2010; Souza and Oberauer, 2014). There are several accounts for the correlation between working memory and temporal characteristics of stimuli. For instance, for Bunting and Cowan’s model (Bunting and Cowan, 2005; Cowan, 2008), it is the passing of time that leads to a progressive deterioration of the working memory, while for other models, it is a distracting stimulus that affects participants’ performance during the tasks (Oberauer et al., 2012; Manohar and Husain, 2016). In contrast to these models that see working memory as being affected by the overall duration of the task (Harrison et al., 2015), models on temporal distinctiveness predict that working memory depends on relative time—that is, the time elapsed since the event to be recovered versus the time elapsed by other potentially interfering events (Souza and Oberauer, 2014). In fact, Oberauer and Lewandowsky showed that representations of different events overlap with each other to the degree that they are similar to each other and occur in close temporal proximity (Oberauer and Lewandowsky, 2013). Another aspect that affects working memory is the rate of stimuli presentation (i.e., the rhythm of a sequence). Some studies show that different rhythms of stimuli presentation compromise participants’ performance due to the unpredictability of events (Lecerf and De Ribaupierre, 2005; Lupo et al., 2018). For instance, Lupo et al. (2018) conducted a study with 71 healthy subjects who completed sequential and simultaneous navigation tests using an innovative sensor platform. They found that the variation in visual stimuli presentation times, without changes in interstimulus intervals, affects performance compared to when presentation times remain unchanged. However, although stimulus temporal unpredictability and stimulus duration both lead to false expectations, they are associated with different brain activations (Liu et al., 2008; Wu et al., 2010; Manohar and Husain, 2016; van Ede et al., 2017). In a recent review of fMRI studies, Mirino et al. (2022) concluded that the principal olivary nucleus (Lewis and Miall, 2003; Liu et al., 2008; Wu et al., 2010) plays a role in detecting temporal irregularity and proposed that this brain area could have a critical role in processing the temporal characteristics of visuospatial information.

In this context, it becomes important to understand the mechanisms underlying the effects of temporal regularity on visuospatial working memory. Therefore, the present study aimed at investigating whether temporal anomalies in the presentation of visual stimuli affect performance at a visuospatial working memory task, when the temporal variation is not part of the response, and it is not part of the attentional set.

We created a computerized Time Squares Sequence, which consists of two sequences of seven white squares, presented in a matrix of gray squares (S1 and S2). Participants responded based on whether the positions of all squares in the second sequence were the same as those in the first sequence. Importantly, we varied both the positions (same and different) and the presentation time of the squares (with and without temporal anomaly) of the two sequences (S1 and S2), leaving the interval between stimuli unchanged. We first report the findings from a pilot study, based on which the number of squares to use in the main study was established, followed by the findings of the main study.

The current study investigated to what extent temporal anomalies in stimuli presentation affect performance when the temporal variation is not part of the response or part of the attentional set.

We used a novel task and examined whether temporal anomalies of visuospatial stimuli with random and unpredictable spans could affect participants’ working memory abilities and, therefore, their performance. In doing so, we also provide a new tool to be used for working memory assessments.

The computerized “Time Squares Sequences” test allowed for the creation of a series of sequences of visuospatial stimuli, in which unbeknownst to participants, the presentation duration of the elements that made up the sequences could be the same (no anomaly) or varied (with anomaly). Participants responded based only on the spatial characteristics of the stimuli.

Our findings showed that response speed but not accuracy was affected by this manipulation, namely, responses were slower in the fixed–variable (FV) than in the fixed–fixed (FF) and the variable–variable (VV) conditions. Importantly, that response speed did not differ between the fixed–fixed and the variable–fixed conditions suggests that it is not the presence of an anomaly but rather the timing of the anomaly that affects performance. In fact, participants were more sensitive to the temporal anomaly when it was present during the recognition phase (i.e., FV and VV conditions), affecting stimulus processing and slowing down responses. This account is in line with a study by Blalock and Clegg (2010), in which the variation in participants’ performance was investigated using a task with simultaneous or delayed sequences of stimuli. Findings showed better performance accuracy in the condition with simultaneous presentation of stimuli. This is because when we store a sequence of events, adding a time variable can affect the encoding. In fact, the literature shows that the simultaneous processing of visuospatial stimuli has a lower attentional and mnemonic load, as stimuli can be viewed as a single pattern (Lupo et al., 2018). On the other hand, different presentation times interfere with the processes of memorization and recognition (Bharti et al., 2020). This is because, compared to a simultaneous presentation, a variable sequence yields a greater cognitive load because, in addition to processing the single stimulus, the time elapsing between stimuli of the entire sequence also needs to be encoded. This greater cognitive load is reflected in poorer performance.

In our study, the timing was always a variable being processed in the coding phase, both when the temporal stimuli presentation was the same, as well as when it was different. Our findings showed that a sudden change in the stimuli presentation timing (i.e., an anomaly) affected only response times when the anomaly occurred during the recognition process (i.e., when S2 was presented). This suggests a mechanism for detecting the changes between the previous and the information that had just been seen (e.g., memorization phase and recognition phase), which operates after the coding phase. This mechanism would allow us to monitor the progress of events over time. However, it is also possible that this mechanism works independently and that, by detecting temporal anomalies, it considers the information only if the stimulus has changed from the one previously encoded.

Importantly, the current findings could guide future research into assessing the anatomical-functional aspects underlying the ability to detect temporal variations of stimuli. Based on extant evidence from fMRI studies, we have proposed that the inferior olive complex has a critical role in processing the temporal characteristics of visuospatial information (Mirino et al., 2022). For instance, such a proposal matches evidence by Xu et al. (2006), who showed the involvement of subcortical areas, including the inferior olive complex, an area located in the brainstem, in processing temporal characteristics of stimuli. Accordingly, future studies could help understand whether the activation of the inferior olive complex, when processing or detecting temporal anomalies, modulates the activation of other brain structures.

In conclusion, the present findings show that the “Time Squares Sequences” may represent an effective tool to evaluate time processing in visuospatial working memory tasks and that it could be also used to investigate underlying neural mechanisms. Moreover, the task can be successfully used to assess changes occurring with aging, as it can provide useful information on how time is processed during the physiological aging of the individual’s brain as well as during pathological aging (e.g., neurodegenerative illnesses) or following brain injury from head trauma (Mirino et al., 2022).

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by the Institutional Review Board of Sapienza University of Rome Department of Psychology (protocol number 0000272 of 17.02.2022).

CG and PM: conceptualization, methodology, test implementation. PM, SM, ADP, and MS: data collection. PM and AP: data analysis. PM and SM: writing—original draft preparation. CG, AP, and MB: writing—review and editing. CG and AP: supervision. CG: project administration. All authors contributed to the article and approved the submitted version.

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.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fnbeh.2023.1165906/full#supplementary-material