Functional interplay between stimulus-oriented and stimulus-independent attending during a prospective memory task
Introduction
Complex situations of everyday life require a continuous alternation between so-called stimulus-independent (SI) and stimulus-oriented (SO) attending (Burgess et al., 2007, Burgess et al., 2005). Attending refers to the allocation of processing resources for the access to central representations in order to execute cognitive tasks. In particular, SO attending enhances our ability to notice changes in the environment when our attention is oriented toward external stimuli experienced through the senses. SI attending is when attention is directed toward self-generated thoughts. The interplay between SO and SI attending is commonplace in multitasking situations, i.e. when a subject performs two or more dovetailed tasks but, due to cognitive constraints, only one task can be performed at any one time (Burgess, Veitch, de Lacy Costello, & Shallice, 2000). PM is a particular condition of multitasking that refers to cognitive processes that underlie the realization of intended actions in the future. In a typical experimental PM event-based paradigm, during an initial encoding phase, an action is linked to a cue that triggers the realization of the intended action (i.e. event-based PM task; Einstein & McDaniel, 1990). The delay between the encoding and the cue presentation should be quite long and filled with a continuous attention-demanding activity called the ongoing (ONG) task that is meant to prevent a continuous rehearsal of the intention (see Burgess, Scott, & Frith, 2003 for key features of a PM task). This particularly fits with ecological situations, whereas experimental paradigms usually require more multitasking abilities because delays are usually shorter and the frequency of PM cues higher. The PM task is formed by distinct components that seems to be mediated by different brain substrates (see West, 2011): the encoding of delayed intentions, the cue identification and the consequent intention retrieval (Einstein, Holland, McDaniel, & Guynn, 1992). These last two components rely on different processes (Cohen, West, & Craik, 2001): the cue identification is influenced by stimulus-driven processes such as saliency or distinctiveness; the intention retrieval is influenced by conceptually-driven processes (Cohen et al., 2001, Mäntylä, 1996), such as the strength of the association between the PM cue and the intention (Cohen et al., 2001, Cohen et al., 2003). Thus, it can be postulated that cue identification involves SO attending more than SI attending, whereas intention retrieval involves SI attending more than SO attending (Simons, Scholvinck, Gilbert, Frith, & Burgess, 2006). Indeed, during an event-based PM task, attention is continuously biased between SO attending for the cue detection and SI attending for the maintenance and the access to the characteristics of the intended actions.
SO and SI attending are thought to be neuro-anatomically as well as behaviourally segregated. Neuropsychological (Burgess et al., 2009, Burgess et al., 2000, Shallice and Burgess, 1991), neuroimaging (Benoit et al., 2012, Burgess et al., 2001, Burgess et al., 2003, den Ouden et al., 2005, Gilbert et al., 2009, Gilbert, 2011, Hashimoto et al., 2011, Haynes et al., 2007, Okuda et al., 1998, Okuda et al., 2007, Poppenk et al., 2010, Reynolds et al., 2009, Simons et al., 2006) and TMS (Costa et al., 2011, Costa et al., 2013) studies reported a consistent relationship between brain activity in Brodmann area 10 (BA10) and PM task performance. In particular, a functional dissociation in BA10 has been proposed within the framework of the gateway hypothesis (Burgess et al., 2005, Burgess et al., 2007). In this view, the lateral portion (latBA10) is mainly involved in SI attending, whereas, the medial BA10 (medBA10) mediates SO attending (Benoit et al., 2012, Simons et al., 2006). According with this view, BA10 acts as a gateway that biases attention between SO and SI attending.
Only two previous functional magnetic resonance imaging (fMRI) studies tested this hypothesis during a PM task (Benoit et al., 2012, Simons et al., 2006). Simons et al. (2006) increased SO attending by presenting PM cues perceptually embedded in the ONG task, and SI attending by increasing the number of actions constituting the delayed intention. During both PM conditions, they showed increased brain activity in latBA10 and decreased brain activity in medBA10 (in agreement with previous neuroimaging studies, cf. Burgess et al., 2003, Okuda et al., 2007). Consistent with the gateway hypothesis, this effect was larger when the intention retrieval demands (i.e. SI attending) were increased. Similarly, Benoit et al. (2012) explored the relationship between the hemodynamic changes in BA10 during PM performance and differences between SI and SO attending conditions. In an fMRI factorial design, they modulated SO-SI attending by asking subjects to execute a task based on visually presented vs. internally generated information (i.e. participants had to picture the visual stimulus in their mind). This was done during an ongoing task alone (ONG) or during a task that also required carrying out a delayed intention (i.e. the PM condition). This study showed that medBA10 was jointly associated with ONG task activity and SO attending. Conversely, left latBA10 showed an effect of PM task, an interaction between PM task and stimulus phase and an effect of switch between SO and SI. These findings are consistent with the proposal that the lateral portion of BA10 is recruited to bias attention toward internal representations.
Nonetheless, these previous studies did not directly address the relative contribution of SO and SI attending specifically on the PM cue identification, which is a central tenet of the gateway hypothesis. Here, to bias attention toward SI attending, we increased the prospective memory Load (i.e. the number of PM cues), whereas to bias attention toward SO attending, we increased the perceptual Saliency of PM cues. Accordingly, we were able to test the gateway hypothesis directly on mechanisms of PM cue identification.
We used an event based PM paradigm that orthogonally crossed three factors in a 2×2×2 design: Task, Saliency and memory Load. Each trial of the ongoing task (ONG) consisted in the presentation of a single letter (first display), followed by a string of 4 letters (second display). The subject was asked to report whether the letter presented in the first display was then shown on the left or the right side of the string in the second display (see Fig. 1). While doing this, the participants also maintained the intention to press a different button, whenever the string in the second display included a specific, pre-defined letter: i.e. the PM cue. The SO attending manipulation consisted of incrementing of the saliency of the ONG targets or the PM cues. We presented PM cues that were either embedded (low saliency) or stood out (high saliency) from distracters. Salient stimuli are distinctive sensory inputs that attract exogenous attention (stimulus-driven attention) (see Corbetta, Patel, & Shulman, 2008). Accordingly, we increased the perceptual distinctiveness of the PM cue and ONG target (Cohen et al., 2003). The SI attending manipulation consisted in changing the number of possible PM cues that the subject had to maintain and respond to (i.e. 1 or 4, pre-defined letters). The high-load condition, with 4 possible PM cues, will bias attention toward internal representations.
Based on the results of previous studies (Benoit et al., 2012, Simons et al., 2006), we expected that medBA10 would show enhanced activity for salient stimuli (SO attending, high saliency), in particular when the salient stimuli were PM cues. We expected that latBA10 would activate upon presentation of the PM cues and, more so, when their number was increased (SI attending, high memory load). We used a functional localizer based on previous literature (Burgess et al., 2003) to independently identify medBA10 and latBA10. In these two regions of interest we tested the main effects of SO and SI attending and their interactions with the PM task. In addition, because recent evidence indicated that medBA10 and latBA10 co-activate with distinct sets of other brain regions (see Gilbert, Gonen-Yaacovi, Benoit, Volle, & Burgess, 2010), here we also tested the effect of SI and SO at the whole-brain level. In particular, together with latBA10, we expected possible influence of SI in the anterior cingulate, insula and fronto-parietal cortex; whereas, together with medBA10, we expected SO to affect also activity in the posterior cingulate and temporal lobe (cf. Gilbert et al., 2010).
Section snippets
Participants
Sixteen right-handed (Edinburgh Inventory; Oldfield, 1971) volunteers (nine females and seven males, aged 18–44 years) with no history of neurological, psychiatric, or visual symptoms participated in the fMRI study. None of the participants was taking vasoactive or psychotropic medication. Written informed consent was obtained from each participant, and the experiment protocol was developed in accordance with the Declaration of Helsinki and was approved by the independent Ethics Committee of
Behavioural data
Memory load and saliency influenced behaviour during PM trials. High memory load decreased accuracy [F(1,15)=8.768, p=.01; Cohen's d=0.4] and increased reaction times of correct responses [F(1,15)=117.376, p<.001; Cohen's d=1.1)]. Conversely, salient PM cues increased accuracy [F(1,15)=11.71, p=.004; Cohen's d=0.4] and decreased reaction times of correct responses [F(1,15)=7.929, p=.013; Cohen's d=0.2]. We found no significant interaction between salience and memory load for either accuracy [F
Discussion
The findings of the present study support the gateway hypothesis about the role of BA10 during a PM task, considering this brain region within a broaden system of networks of areas. We found that in the left hemisphere, BOLD activity in latBA10 and in a network of dorso-lateral fronto-parietal regions was transiently enhanced by the presentation on PM cues when memory Load was increased. This effect did not reach significance in the right lateral BA10, consistent with previous findings of a
Conclusions
The present study showed a functional segregation between medBA10 and latBA10 that mediate SO and SI attending respectively. These findings are consistent with the gateway hypothesis. We suggest that medBA10 and latBA10 are parts of different large-scale brain networks, such as the default mode and the attentional network. They are involved respectively in baseline brain activity, mediating the processing of salient external stimuli, versus attention demanding tasks, which are influenced by
Acknowledgments
An extended abstract of preliminary data of the present study has been published in Behavioural Neurology (2012, May 24) after its presentation at the 3rd meeting of the Federation of European Societies of Neuropsychology (ESN) in Basel, Switzerland.
References (48)
- et al.
The gateway hypothesis of rostral prefrontal cortex (area 10) function
Trends in Cognitive Sciences
(2007) - et al.
Functional neuroimaging studies of prospective memory: What have we learnt so far?
Neuropsychologia
(2011) - et al.
Brain regions involved in prospective memory as determined by positron emission tomography
Neuropsychologia
(2001) - et al.
The role of the rostral frontal cortex (area 10) in prospective memory: A lateral versus medial dissociation
Neuropsychologia
(2003) - et al.
The cognitive and neuroanatomical correlates of multitasking
Neuropsychologia
(2000) - et al.
The reorienting system of the human brain: From environment to theory of mind
Neuron
(2008) - et al.
Thinking about intentions
NeuroImage
(2005) - et al.
Classical and Bayesian inference in neuroimaging: Applications
NeuroImage
(2002) - et al.
Distinct functional connectivity associated with lateral versus medial rostral prefrontal cortex: A meta-analysis
NeuroImage
(2010) - et al.
Neural substrates of implicit cueing effect on prospective memory
NeuroImage
(2011)
Reading hidden intentions in the human brain
Current Biology: CB
Precentral gyrus discrepancy in electronic versions of the Talairach atlas
NeuroImage
An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets
NeuroImage
Differential involvement of regions of rostral prefrontal cortex (Brodmann area 10) in time- and event-based prospective memory
International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology
Participation of the prefrontal cortices in prospective memory: Evidence from a PET study in humans
Neuroscience Letters
The assessment and analysis of handedness: The Edinburgh inventory
Neuropsychologia
Encoding the future: Successful processing of intentions engages predictive brain networks
NeuroImage
Differential components of prospective memory? Evidence from fMRI
Neuropsychologia
The temporal dynamics of prospective memory: A review of the ERP and prospective memory literature
Neuropsychologia
Rostral prefrontal cortex and the focus of attention in prospective memory
Cerebral Cortex
Individual differences in event-based prospective memory: Evidence for multiple processes supporting cue detection
Memory & Cognition
Mesulam's frontal lobe mystery re-examined
Restorative Neurology and Neuroscience
The gateway hypothesis of rostral prefrontal cortex (area 10) function
The effect of perceptual distinctiveness on the prospective and retrospective components of prospective memory in young and old adults
Canadian Journal of Experimental Psychology=Revue Canadienne De Psychologie Experimentale
Cited by (22)
Sensory modality affects the spatiotemporal dynamics of alpha and theta oscillations associated with prospective memory
2024, International Journal of PsychophysiologyTheta and alpha oscillations as signatures of internal and external attention to delayed intentions: A magnetoencephalography (MEG) study
2020, NeuroImageCitation Excerpt :This pattern has been interpreted within the ‘gateway hypothesis’ framework (Burgess et al., 2007; Gilbert et al., 2005; Henseler et al., 2011), according to which lateral and medial aPFC regions are deputed to stimulus-independent and stimulus-oriented processes, respectively. Lateral and medial aPFC regions would thus act to direct the attention between the internally representation of PM intention and the external stimuli (Barban et al., 2013, 2014; Henseler et al., 2011). All these findings have been obtained, however, by using fMRI: a neuroimaging technique characterized by good spatial resolution but poor temporal resolution.
Superior parietal cortex and the attention to delayed intention: An rTMS study
2017, NeuropsychologiaCitation Excerpt :One of the key regions supporting PM is the anterior prefrontal cortex (aPFC; Brodmann Area, BA 10), which acts as a gateway mechanism between stimulus-independent and stimulus-oriented thoughts (Burgess et al., 2007, 2011; Gilbert et al., 2005). More specifically, the lateral parts of the aPFC mediate stimulus-independent processes, which include maintaining the PM intention active in memory, whereas the medial parts of the aPFC support stimulus-oriented processes, such as processing of the ongoing stimuli (Barban et al., 2014; Benoit et al., 2012; Burgess et al., 2007, 2011; Gilbert et al., 2005, 2006). In such a way, aPFC regions orchestrate and distribute the resources allocated for the PM task and the ongoing activity, allowing an individual to perform both tasks simultaneously.
Neural bases of prospective memory: A meta-analysis and the "Attention to Delayed Intention" (AtoDI) model
2015, Neuroscience and Biobehavioral ReviewsCitation Excerpt :More specifically, medial aPFC would be engaged in supporting SO attending whereas lateral aPFC would mediate SI attending (Burgess et al., 2007). A recent study tested this hypothesis directly within the PM context, by manipulating the salience of the PM cue and the memory load of PM task (Barban et al., 2014). The findings corroborated the Gateway Hypothesis, revealing that the medial aPFC showed enhanced activity for highly salient PM cues, which stress SO attending, whereas the lateral aPFC showed increased activity especially for high memory load, which emphasizes SI attending.