Dopaminergic and cholinergic modulations of visual-spatial attention and working memory: insights from molecular genetic research and implications for adult cognitive development

Attention and working memory are fundamental for selecting and maintaining behaviorally relevant information. Not only do both processes closely intertwine at the cognitive level, but they implicate similar functional brain circuitries, namely the frontoparietal and the frontostriatal networks, which are innervated by cholinergic and dopaminergic pathways. Here we review the literature on cholinergic and dopaminergic modulations of visual-spatial attention and visual working memory processes to gain insights on aging-related changes in these processes. Some extant findings have suggested that the cholinergic system plays a role in the orienting of attention to enable the detection and discrimination of visual information, whereas the dopaminergic system has mainly been associated with working memory processes such as updating and stabilizing representations. However, since visual-spatial attention and working memory processes are not fully dissociable, there is also evidence of interacting cholinergic and dopaminergic modulations of both processes. We further review gene-cognition association studies that have shown that individual differences in visual-spatial attention and visual working memory are associated with acetylcholine- and dopamine-relevant genes. The efficiency of these 2 transmitter systems declines substantially during healthy aging. These declines, in part, contribute to age-related deficits in attention and working memory functions. We report novel data showing an effect of dopamine COMT gene on spatial updating processes in older but not in younger adults, indicating potential magnification of genetic effects in old age.     

Cross-modal working memory binding and L1-L2 word learning

The ability to create temporary binding representations of information from different sources in working memory has recently been found to relate to the development of monolingual word recognition in children. The current study explored this possible relationship in an adult word-learning context. We assessed whether the relationship between cross-modal working memory binding and lexical development would be observed in the learning of associations between unfamiliar spoken words and their semantic referents, and whether it would vary across experimental conditions in first- and second-language word learning. A group of English monolinguals were recruited to learn 24 spoken disyllable Mandarin Chinese words in association with either familiar or novel objects as semantic referents. They also took a working memory task in which their ability to temporarily bind auditory-verbal and visual information was measured. Participants’ performance on this task was uniquely linked to their learning and retention of words for both novel objects and for familiar objects. This suggests that, at least for spoken language, cross-modal working memory binding might play a similar role in second language-like (i.e., learning new words for familiar objects) and in more native-like situations (i.e., learning new words for novel objects). Our findings provide new evidence for the role of cross-modal working memory binding in L1 word learning and further indicate that early stages of picture-based word learning in L2 might rely on similar cognitive processes as in L1.     

Spatial and visual working memory ability in children with difficulties in arithmetic word problem solving

Although various studies support the multicomponent nature of visuospatial working memory, to date there is no general consensus on the distinction of its components. A difference is usually proposed between visual and spatial components of working memory, but the individual roles of these components in mathematical learning disabilities remains unclear. The present study aimed to examine the involvement of visual and spatial working memory in poor problem-solvers compared with children with normal level of achievement. Fourth-grade participants were presented with tasks measuring phonological loop, central executive, and visual versus spatial memory. In two separate experiments, both designed to distinguish visual and spatial component involvement, poor problem-solvers specifically failed on spatial—but not visual or phonological—working memory tasks. Results are discussed in the light of possible working memory models, and specifically demonstrate that problem-solving ability can benefit from analysis of spatial processes, which involves ability to manipulate and transform relevant information; instead, no benefit is gained from the analysis of visual pictorial detail.     

Ageing and feature binding in visual working memory: The role of presentation time

A large body of research has clearly demonstrated that healthy ageing is accompanied by an associative memory deficit. Older adults exhibit disproportionately poor performance on memory tasks requiring the retention of associations between items (e.g., pairs of unrelated words). In contrast to this robust deficit, older adults’ ability to form and temporarily hold bound representations of an object's surface features, such as colour and shape, appears to be relatively well preserved. However, the findings of one set of experiments suggest that older adults may struggle to form temporary bound representations in visual working memory when given more time to study objects. However, these findings were based on between-participant comparisons across experimental paradigms. The present study directly assesses the role of presentation time in the ability of younger and older adults to bind shape and colour in visual working memory using a within-participant design. We report new evidence that giving older adults longer to study memory objects does not differentially affect their immediate memory for feature combinations relative to individual features. This is in line with a growing body of research suggesting that there is no age-related impairment in immediate memory for colour-shape binding.     

Automatic guidance of attention from working memory

Recent research has shown interactions between the process of keeping information 'online' in working memory, and the processes that select relevant information for a response. In particular, our ability to select stimuli in the environment can be modulated by whether the stimuli match the current contents of working memory. Guidance of selection from working memory occurs automatically, even when it is detrimental to performance. Neurophysiological data, from functional brain imaging, indicate that the interaction between working memory and attention is based on neuronal mechanisms distinct from the processes mediating 'bottom-up' priming effects from implicit memory. We discuss the importance of 'top-down' influences from working memory on the 'early' deployment of attention and on the processes that gate visual information into awareness.     

You’re looking for what? Comparing search for familiar,nameable objects to search for unfamiliar,novel objects

Searching for items in one’s environment often includes considerable reliance on semantic knowledge. The present study examines the importance of semantic information in visual and memory search, especially with respect to whether the items reside in long-term or working memory. In Experiment 1, participants engaged in hybrid visual memory search for items that were either highly familiar or novel. Importantly, the relatively large number of targets in this hybrid search task necessitated that targets be stored in some form of long-term memory. We found that search for familiar objects was more efficient than search for novel objects. In Experiment 2, we investigated search for familiar versus novel objects when the number of targets was low enough to be stored in working memory. We also manipulated how often participants in Experiment 2 were required to update their target (every trial vs. every block) in order to control for target templates that were stored in long-term memory as a result of repeated exposure over trials. We found no differences in search efficiency for familiar versus novel objects when templates were stored in working memory. Our results suggest that while semantic information may provide additional individuating features that are useful for object recognition in hybrid search, this information could be irrelevant or even distracting when searching for targets stored in working memory.     

Visual search is slowed when visuospatial working memory is occupied

Visual working memory plays a central role in most models of visual search. However, a recent study showed that search efficiency was not impaired when working memory was filled to capacity by a concurrent object memory task (Woodman, Vogel, & Luck, 2001). Objects and locations may be stored in separate working memory subsystems, and it is plausible that visual search relies on the spatial subsystem, but not on the object subsystem. In the present study, we sought to determine whether maintaining spatial information in visual working memory impairs the efficiency of a concurrent visual search task. Visual search efficiency and spatial memory accuracy were both impaired when the search and the memory tasks were performed concurrently, as compared with when the tasks were performed separately. These findings suggest that common mechanisms are used to process information during difficult visual search tasks and to maintain spatial information in working memory.     

Working memory capacity predicts search accuracy for novel as well as repeated targets

Visual search behaviour is guided by mental representations of targets that direct attention toward relevant features in the environment. Electrophysiological data suggests these target templates are maintained by visual working memory during search for novel targets and rapidly transfer to long term memory with target repetition. If this account is correct, an individual’s working memory capacity should be more predictive of search performance for novel targets than repeated targets. Across six experiments, we tested this hypothesis using both single (Experiments 5 and 6) and multiple (Experiments 1–4) target search tasks with three different types of stimuli (real world objects, letters, and triple conjunction shapes). Each target set was repeated for six consecutive trials. In addition, we estimated visual working memory capacity using a change detection working memory task. Overall, working memory capacity did not predict response time or efficiency in the visual search task. However, working memory capacity was equally predictive of search accuracy for both novel and repeated targets. These results suggest that working memory requirements do not substantially differ between novel and repeated target search, and working memory capacity may continue to play an important role in the encoding or maintenance of target representations after they are presumed to be in long term memory.     

Do the contents of visual working memory automatically influence attentional selection during visual search?

In many theories of cognition, researchers propose that working memory and perception operate interactively. For example, in previous studies researchers have suggested that sensory inputs matching the contents of working memory will have an automatic advantage in the competition for processing resources. The authors tested this hypothesis by requiring observers to perform a visual search task while concurrently maintaining object representations in visual working memory. The hypothesis that working memory activation produces a simple but uncontrollable bias signal leads to the prediction that items matching the contents of working memory will automatically capture attention. However, no evidence for automatic attentional capture was obtained; instead, the participants avoided attending to these items. Thus, the contents of working memory can be used in a flexible manner for facilitation or inhibition of processing.     

Interactions between visual working memory and selective attention

The relationship between working memory and selective attention has traditionally been discussed as operating in one direction: Attention filters incoming information, allowing only relevant information into short-term processing stores. This study tested the prediction that the contents of visual working memory also influence the guidance of selective attention. Participants held a sample object in working memory on each trial. Two objects, one matching the sample and the other novel, were then presented simultaneously. As measured by a probe task, attention shifted to the object matching the sample. This effect generalized across object type, attentional-probe task, and working memory task. In contrast, a matched task with no memory requirement showed the opposite pattern, demonstrating that this effect is not simply due to exposure to the sample. These results confirm a specific prediction about the influence of working memory contents on the guidance of attention.     

Do binding deficits account for age-related decline in visual working memory?

Remembering visual material, such as objects, faces, and spatial locations, over a short period of time (seconds) becomes more difficult as we age. We investigated whether these deficits could be explained by a simple reduction in visual working memory capacity or by an impairment in one's ability to form or maintain appropriate associations among pieces of related information. In three experiments, we used recognition and recall tests to address the efficacy with which older adults can create bound object representations by varying the number of features of each object that had to be remembered for a subsequent memory test. Results demonstrated that whereas older adults exhibited reduced memory capacity as compared with that of younger adults, both groups stored integrated object representations in visual working memory. These results are contrasted with other work that suggests that age-related memory decline is due, at least in part, to associative deficits.     

Visual and verbal working memory loads interfere with scene-viewing

Working memory is thought to be divided into distinct visual and verbal subsystems. Studies of visual working memory frequently use verbal working memory tasks as control conditions and/or use articulatory suppression to ensure that visual load is not transferred to verbal working memory. Using these verbal tasks relies on the assumption that the verbal working memory load will not interfere with the same processes as visual working memory. In the present study, participants maintained a visual or verbal working memory load as they simultaneously viewed scenes while their eye movements were recorded. Because eye movements and visual working memory are closely linked, we anticipated the visual load would interfere with scene-viewing (and vice versa), while the verbal load would not. Surprisingly, both visual and verbal memory loads interfered with scene-viewing behavior, while eye movements during scene-viewing did not significantly interfere with performance on either memory task. These results suggest that a verbal working memory load can interfere with eye movements in a visual task.

     

Visual short-term memory load suppresses temporo-parietal junction activity and induces inattentional blindness

The right temporo-parietal junction (TPJ) is critical for stimulus-driven attention and visual awareness. Here we show that as the visual short-term memory (VSTM) load of a task increases, activity in this region is increasingly suppressed. Correspondingly, increasing VSTM load impairs the ability of subjects to consciously detect the presence of a novel, unexpected object in the visual field. These results not only demonstrate that VSTM load suppresses TPJ activity and induces inattentional blindness, but also offer a plausible neural mechanism for this perceptual deficit: suppression of the stimulus-driven attentional network.     

The scope and control of attention as separate aspects of working memory

The present study examines two varieties of working memory (WM) capacity task: visual arrays (i.e., a measure of the amount of information that can be maintained in working memory) and complex span (i.e., a task that taps WM-related attentional control). Using previously collected data sets we employ confirmatory factor analysis to demonstrate that visual arrays and complex span tasks load on separate, but correlated, factors. A subsequent series of structural equation models and regression analyses demonstrate that these factors contribute both common and unique variance to the prediction of general fluid intelligence (Gf). However, while visual arrays does contribute uniquely to higher cognition, its overall correlation to Gf is largely mediated by variance associated with the complex span factor. Thus we argue that visual arrays performance is not strictly driven by a limited-capacity storage system (e.g., the focus of attention; Cowan, 2001), but may also rely on control processes such as selective attention and controlled memory search.     

A two-stage search of visual working memory: investigating speed in the change-detection paradigm

A popular procedure for investigating working memory processes has been the visual change-detection procedure. Models of performance based on that procedure, however, tend to be based on performance accuracy and treat working memory search as a one-step process, in which memory representations are compared to a test probe to determine if a match is present. To gain a clearer understanding of how search of these representations operate in the change-detection task, we examined reaction time in two experiments, with a single-item probe either located centrally or at the location of an array item. Contrary to current models of visual working memory capacity, our data point to a two-stage search process: a fast first step to check for the novelty of the probe and, in the absence of such novelty, a second, slower step to search exhaustively for a match between the test probe and a memory representation. In addition to these results, we found that participants tended not to use location information provided by the probe that theoretically could have abbreviated the search process. We suggest some basic revisions of current models of processing in this type of visual working memory task.     

Gender differences in episodic memory and visual working memory including the effects of age

Analysing the relationship between gender and memory, and examining the effects of age on the overall memory-related functioning, are the ongoing goals of psychological research. The present study examined gender and age group differences in episodic memory with respect to the type of task. In addition, these subgroup differences were also analysed in visual working memory. A sample of 366 women and 330 men, aged between 16 and 69 years of age, participated in the current study. Results indicate that women outperformed men on auditory memory tasks, whereas male adolescents and older male adults showed higher level performances on visual episodic and visual working memory measures. However, the size of gender-linked effects varied somewhat across age groups. Furthermore, results partly support a declining performance on episodic memory and visual working memory measures with increasing age. Although age-related losses in episodic memory could not be explained by a decreasing verbal and visuospatial ability with age, women's advantage in auditory episodic memory could be explained by their advantage in verbal ability. Men's higher level visual episodic memory performance was found to result from their advantage in visuospatial ability. Finally, possible methodological, biological, and cognitive explanations for the current findings are discussed.     

Examining inhibition of return with multiple sequential cues in younger and older adults

Studies with younger adults have shown that when multiple peripheral cues are presented sequentially, inhibition of return (IOR) occurs at several locations with the greatest IOR at the most recently cued location and the least at the earliest cued location. The inhibitory ability needed to tag multiple locations requires visuospatial working memory, and it is thought that this type of memory may be vulnerable to the effects of aging. The present experiments examined whether older adults would show less IOR at multiple cued locations than younger adults when placeholders were present (Experiment 1) and absent (Experiment 2). Of interest, in both experiments older adults showed an almost identical pattern of IOR, in both magnitude and number of inhibited locations, to that of younger adults. This finding, in conjunction with research on memory-guided saccades, suggests that there may be a form of visuospatial working memory, specific to oculomotor and visual attention processes, that is relatively resistant to the effects of aging.     

Impaired discourse gist and working memory in children after brain injury

Emerging evidence suggests that a traumatic brain injury (TBI) in childhood may disrupt the ability to abstract the central meaning or gist-based memory from connected language (discourse). The current study adopts a novel approach to elucidate the role of immediate and working memory processes in producing a cohesive and coherent gist-based text in the form of a summary in children with mild and severe TBI as compared to typically developing children, ages 8-14 years at test. Both TBI groups showed decreased performance on a summary production task as well as retrieval of specific content from a long narrative. Working memory on n-back tasks was also impaired in children with severe TBI, whereas immediate memory performance for recall of a simple word list in both TBI groups was comparable to controls. Interestingly, working memory, but not simple immediate memory for a word list, was significantly correlated with summarization ability and ability to recall discourse content.     

Activation of the opioid and nonopioid analgesic systems: evidence for a memory hypothesis and against the coulometric hypothesis

It has been suggested that the magnitude and form of hypoalgesia elicited by an aversive event can be predicted from its coulometric product (Intensity X Duration). According to this hypothesis, small products elicit opioid hypoalgesia, and large products elicit nonopioid hypoalgesia. This suggests that increasing the duration of an aversive event should heighten the nonopioid hypoalgesia. Contrary to this prediction, in Experiment 1 I found that increasing the duration of a mild shock attenuated the nonopioid hypoalgesia. In Experiment 2 I tested another implication of the coulometric hypothesis, namely, that mild shocks that have the same coulometric product should elicit equivalent hypoalgesia. The results did not support this prediction. We discuss how these findings are consistent with an alternative theory, the "working memory hypothesis." According to this theory, the representation of an aversive event in working memory elicits hypoalgesia. In Experiment 3 a novel prediction of this theory was tested, namely, that displacing the representation of intense shock from working memory, by following the intense shock with a weak shock "distractor", should attenuate hypoalgesia. The results support this prediction. I conclude by discussing the relation of this work to other findings in the analgesia literature.     

Adapting a memory framework (source monitoring) to the study of closure processes

The present experiments adapt a memory framework (source monitoring) to the study of closure processes. Closure processes are invoked as explanatory mechanisms underlying the ability to identify objects under conditions of incomplete visual information. If closure processes are activated, filling in missing pieces of visual information, intriguing memory predictions follow. When making source judgments about the way in which visual information was experienced initially (e.g., complete or incomplete in form), a particular kind of memory error should be evident. Incomplete visual information should be remembered as complete in form, and indeed, this error is observed. The present experiments test alternative interpretations for the initial reports of this memory error in the context of a search task modeled after the Where's Waldo? children's books. The effects of several new factors (e.g., familiarity) are reported, and alternative interpretations for the bias to report complete are eliminated. Findings, therefore, have implications for understanding the mechanisms of closure processes, as well as for the source-monitoring framework itself.