Kevin T. Jones

tDCS selectively improves working memory in older adults with more education

Cognitive performance, including performance on working memory (WM) tasks declines with age. Changes in brain activations are one presumed contributor to WM decline in the healthy aging population. In particular, neuroimaging studies show that when older adults perform WM tasks there tends to be greater bilateral frontal activity than in younger adults. We hypothesized that stimulating the prefrontal cortex in healthy older adults would improve WM performance. To test this hypothesis we employed transcranial direct current stimulation (tDCS), a neurostimulation technique in which small amounts of electrical current are applied to the scalp with the intent of modulating the activity in underlying neurons. Across three testing sessions we applied sham stimulation or anodal tDCS to the left (F3) or right (F4) prefrontal cortex to healthy older adults as they performed trials of verbal and visual 2-back WM tasks. Surprisingly, tDCS was uniformly beneficial across site and WM task, but only in older adults with more education. In the less educated group, tDCS provided no benefit to verbal or visual WM performance. We interpret these findings as evidence for differential frontal recruitment as a function of strategy when older adults perform WM tasks.

Hits and misses: leveraging tDCS to advance cognitive research

The popularity of non-invasive brain stimulation techniques in basic, commercial, and applied settings grew tremendously over the last decade. Here, we focus on one popular neurostimulation method: transcranial direct current stimulation (tDCS). Many assumptions regarding the outcomes of tDCS are based on the results of stimulating motor cortex. For instance, the primary motor cortex is predictably suppressed by cathodal tDCS or made more excitable by anodal tDCS. However, wide-ranging studies testing cognition provide more complex and sometimes paradoxical results that challenge this heuristic. Here, we first summarize successful efforts in applying tDCS to cognitive questions, with a focus on working memory (WM). These recent findings indicate that tDCS can result in cognitive task improvement or impairment regardless of stimulation site or direction of current flow. We then report WM and response inhibition studies that failed to replicate and/or extend previously reported effects. From these opposing outcomes, we present a series of factors to consider that are intended to facilitate future use of tDCS when applied to cognitive questions. In short, common pitfalls include testing too few participants, using insufficiently challenging tasks, using heterogeneous participant populations, and including poorly motivated participants. Furthermore, the poorly understood underlying mechanism for long-lasting tDCS effects make it likely that other important factors predict responses. In conclusion, we argue that although tDCS can be used experimentally to understand brain function its greatest potential may be in applied or translational research.

Parietal Contributions to Visual Working Memory Depend on Task Difficulty

The nature of parietal contributions to working memory (WM) remain poorly understood but of considerable interest. We previously reported that posterior parietal damage selectively impaired WM probed by recognition (Berryhill and Olson, 2008a). Recent studies provided support using a neuromodulatory technique, transcranial direct current stimulation (tDCS) applied to the right parietal cortex (P4). These studies confirmed parietal involvement in WM because parietal tDCS altered WM performance: anodal current tDCS improved performance in a change detection task, and cathodal current tDCS impaired performance on a sequential presentation task. Here, we tested whether these complementary results were due to different degrees of parietal involvement as a function of WM task demands, WM task difficulty, and/or participants’ WM capacity. In Experiment 1, we applied cathodal and anodal tDCS to the right parietal cortex and tested participants on both previously used WM tasks. We observed an interaction between tDCS (anodal, cathodal), WM task difficulty, and participants’ WM capacity. When the WM task was difficult, parietal stimulation (anodal or cathodal) improved WM performance selectively in participants with high WM capacity. In the low WM capacity group, parietal stimulation (anodal or cathodal) impaired WM performance. These nearly equal and opposite effects were only observed when the WM task was challenging, as in the change detection task. Experiment 2 probed the interplay of WM task difficulty and WM capacity in a parametric manner by varying set size in the WM change detection task. Here, the effect of parietal stimulation (anodal or cathodal) on the high WM capacity group followed a linear function as WM task difficulty increased with set size. The low WM capacity participants were largely unaffected by tDCS. These findings provide evidence that parietal involvement in WM performance depends on both WM capacity and WM task demands. We discuss these findings in terms of alternative WM strategies employed by low and high WM capacity individuals. We speculate that low WM capacity individuals do not recruit the posterior parietal lobe for WM tasks as efficiently as high WM capacity individuals. Consequently, tDCS provides greater benefit to individuals with high WM capacity.

Longitudinal Neurostimulation in Older Adults Improves Working Memory

An increasing concern affecting a growing aging population is working memory (WM) decline. Consequently, there is great interest in improving or stabilizing WM, which drives expanded use of brain training exercises. Such regimens generally result in temporary WM benefits to the trained tasks but minimal transfer of benefit to untrained tasks. Pairing training with neurostimulation may stabilize or improve WM performance by enhancing plasticity and strengthening WM-related cortical networks. We tested this possibility in healthy older adults. Participants received 10 sessions of sham (control) or active (anodal, 1.5 mA) tDCS to the right prefrontal, parietal, or prefrontal/parietal (alternating) cortices. After ten minutes of sham or active tDCS, participants performed verbal and visual WM training tasks. On the first, tenth, and follow-up sessions, participants performed transfer WM tasks including the spatial 2-back, Stroop, and digit span tasks. The results demonstrated that all groups benefited from WM training, as expected. However, at follow-up 1-month after training ended, only the participants in the active tDCS groups maintained significant improvement. Importantly, this pattern was observed for both trained and transfer tasks. These results demonstrate that tDCS-linked WM training can provide long-term benefits in maintaining cognitive training benefits and extending them to untrained tasks.

Differential Frontal Involvement in Shifts of Internal and Perceptual Attention

BACKGROUND Perceptual attention enhances the processing of items in the environment, whereas internal attention enhances processing of items encoded in visual working memory. In perceptual and internal attention cueing paradigms, cues indicate the to-be-probed item before (pre-cueing) or after (retro-cueing) the memory display, respectively. Pre- and retro-cues confer similar behavioral accuracy benefits (pre-: 14-19%, retro-: 11-17%) and neuroimaging data show that they activate overlapping frontoparietal networks. Yet reports of behavioral and neuroimaging differences suggest that pre- and retro-cueing differentially recruit frontal and parietal cortices (Lepsien and Nobre, 2006). OBJECTIVE/HYPOTHESIS This study examined whether perceptual and internal attention are equally disrupted by neurostimulation to frontal and parietal cortices. We hypothesized that neurostimulation applied to frontal cortex would disrupt internal attention to a greater extent than perceptual attention. METHODS Cathodal transcranial direct current stimulation (tDCS) was applied to frontal or parietal cortices. After stimulation, participants completed a change detection task coupled with either pre- or retro-cues. RESULTS Cathodal tDCS across site (frontal, parietal) hindered performance. However, frontal tDCS had a greater negative impact on the retro-cued trials demonstrating greater frontal involvement during shifts of internal attention. CONCLUSIONS These results complement the neuroimaging data and provide further evidence suggesting that perceptual and internal attention are not identical processes. We conclude that although internal and perceptual attention are mediated by similar frontoparietal networks, the weight of contribution of these structures differs, with internal attention relying more heavily on the frontal cortex.

Enhanced long-term memory encoding after parietal neurostimulation

Neurostimulation, e.g., transcranial direct current stimulation (tDCS), shows promise as an effective cognitive intervention. In spite of low spatial resolution, limited penetration, and temporary influence, evidence highlights tDCS-linked cognitive benefits in a range of cognitive domains. The left posterior parietal cortex (PPC) is an accessible node in frontoparietal networks engaged during long-term memory (LTM). Here, we tested the hypothesis that tDCS can facilitate LTM by pairing LTM encoding and retrieval with PPC stimulation. Healthy young adults performed a verbal LTM task (California Verbal Learning Task) with four different stimulation parameters. In Experiment 1, we applied tDCS to left PPC during LTM encoding. In Experiment 2, we applied tDCS just prior to retrieval to test the temporal specificity of tDCS during a LTM task. In later experiments, we tested hemispheric specificity by replicating Experiment 1 while stimulating the right PPC. Experiment 1 showed that tDCS applied during LTM encoding improved the pace of list learning and enhanced retrieval after a short delay. Experiment 2 indicated anodal left PPC tDCS only improved LTM when applied during encoding, and not during maintenance. Experiments 3 and 4 confirmed that tDCS effects were hemisphere specific and that no effects were found after right PPC stimulation during encoding. These findings indicate that anodal tDCS to the PPC helps verbal LTM in healthy young adults under certain conditions. First, when it is applied to the left, not the right, PPC and second, when it is applied during encoding.

Correction: Longitudinal Neurostimulation in Older Adults Improves Working Memory

Fig 4 was incorrectly published as a duplicate of Fig 4. Please see the corrected Fig 4 here. Fig 4 Performance gains per task.

Frontoparietal neurostimulation modulates working memory training benefits and oscillatory synchronization

There is considerable interest in maintaining working memory (WM) because it is essential to accomplish most cognitive tasks, and it is correlated with fluid intelligence and ecologically valid measures of daily living. Toward this end, WM training protocols aim to improve WM capacity and extend improvements to unpracticed domains, yet success is limited. One emerging approach is to couple WM training with transcranial direct current stimulation (tDCS). This pairing of WM training with tDCS in longitudinal designs promotes behavioral improvement and evidence of transfer of performance gains to untrained WM tasks. However, the mechanism(s) underlying tDCS-linked training benefits remain unclear. Our goal was to gain purchase on this question by recording high-density EEG before and after a weeklong WM training+tDCS study. Participants completed four sessions of frontoparietal tDCS (active anodal or sham) during which they performed a visuospatial WM change detection task. Participants who received active anodal tDCS demonstrated significant improvement on the WM task, unlike those who received sham stimulation. Importantly, this pattern was mirrored by neural correlates in spectral and phase synchrony analyses of the HD-EEG data. Notably, the behavioral interaction was echoed by interactions in frontal-posterior alpha band power, and theta and low alpha oscillations. These findings indicate that one mechanism by which paired tDCS+WM training operates is to enhance cortical efficiency and connectivity in task-relevant networks.

Influences on the beneficial effect of neurostimulation

Neurostimulation, such as transcranial direct current stimulation (tDCS) shows promise in improving and maintaining cognition in both neurotypical and patient populations. This technique administers small amounts of electric current through the cortex to modulate the excitability of underlying neurons (Nitsche & Paulus, 2000, 2001). tDCS has some advantages over other neuroimaging and neurostimulation techniques because it is safe, well tolerated, and more affordable. However, recent findings suggest that tDCS may not work equally well across all individuals. First, we administered anodal tDCS to the prefrontal cortex (PFC) in healthy older adults prior to performing a WM task. Interestingly, we found that only the more educated half of our participants showed a WM benefit following tDCS (Berryhill & Jones, 2012). Second, in young adults, we found that right posterior parietal cortex (PPC) tDCS prior to a visual WM recognition task benefited participants with a high WMC (WMC) only (Jones & Berryhill, 2012). The question emerged as to why group differences would predict WM benefits following tDCS. We hypothesize that these findings demonstrated differences in strategy and motivation level in WM tasks across our participants. Previous research implicates differential WM strategy use between participants with a high and low WMC. Those with lower WM capacities are more distractible (Unsworth, 2007), and have fewer attentional resources. Furthermore, high WMC participants are more likely to adopt efficient strategies (Schelble, Therriault, & Miller, 2012). However, when provided effective

Childhood Memory: An Update from the Cognitive Neuroscience Perspective

Children are not simply miniature adults. As such, the memory of a child is significantly different from the memory of an adult. Furthermore, the ability to form memories is not innate and instead develops over the first nearly two decades of life. Consequently, memory researchers working in the developmental domain must carefully design studies to probe memory function using age-appropriate paradigms. This is especially true given the growing range of experimental approaches that can be leveraged to understand the neural underpinnings of memory and its development. Techniques such as functional near-infrared spectroscopy (fNIRS), functional magnetic resonance imaging (fMRI), and high-density electroencephalography (HD-EEG) join workhorse behavioral and neuropsychological methodologies to monitor many aspects of brain function and behavior during memory formation and retrieval.