Improving working memory: Exploring the effect of transcranial random noise stimulation and transcranial direct current stimulation on the dorsolateral prefrontal cortex
Highlights
► Anodal tDCS improves speed of accuracy of WM performance on the 2-back task. ► tRNS does not affect WM performance. ► Anodal tDCS may have significant implications for WM remediation in psychiatric conditions, particularly schizophrenia.
Introduction
Working memory (WM) is the process of temporary storage and processing of information under our attentional control that underpins complex cognitive actions including learning, reasoning, and language (Baddeley, 1992) and thus plays a critical role in cognitive processes necessary for everyday life. Neuroimaging studies indicate that WM is distributed across multiple regions in the brain with increased activity seen on functional imaging studies in specific areas, notably the dorsolateral region of the prefrontal cortex (DLPFC) (D’Esposito and Postle, 1999, Mull and Seyal, 2001, Nyberg and Cabeza, 2000, Postle, 2006, Smith and Jonides, 1997). Deficits in WM are seen in a number of neurological and psychiatric disorders, including schizophrenia, Alzheimer’s disease, Parkinson’s disease, and major depression (Goldman-Rakic, 1994, Morris, 1994, Winograd-Gurvich et al., 2006). To date, the most common approach to addressing WM deficits have been either pharmacological or cognitive rehabilitation. A number of studies have investigated the effects of pharmacotherapy (antipsychotics and anticholinergics) on cognition in schizophrenia for example. The results of such studies are mixed, however, and by and large the effects of these drugs on cognition appear to be limited (Marder, 2006, Penn et al., 1995). Cognitive rehabilitation incorporates strategies for improving memory such as mnemonic encoding and encoding and retrieval practice exercises and has been found to improve WM, but extensive practice is required for moderate improvements at best (McGurk et al., 2007). Therefore, there is a need for new and better treatments of WM deficits. Recent research into the effects of non-invasive methods of brain stimulation on cognitive performance has presented a possible way to do this. Transcranial direct current stimulation (tDCS) is a non-invasive and non-convulsive stimulation technique which shows promise as a treatment for WM deficits (Floel and Cohen, 2007, Fregni et al., 2005). TDCS alters cortex excitability through modulating, rather than directly stimulating, neuronal activity (Nitsche et al., 2008). A small direct electrical current, typically 1–2 mA is induced across the brain from an anode to a cathode electrode (Floel and Cohen, 2007). The excitability of neurons near the scalp is increased or decreased by de- or hyperpolarization of the membrane resting potential. This most likely occurs by modulating the sodium and calcium channels, thus increasing or decreasing the firing rate of the neurons depending upon their alignment with the current flow (Liebetanz et al., 2001, Nitsche et al., 2003). Electrical stimulation of the brain may be delivered in several current profiles including direct, intermittent and random stimulation. Direct current stimulation is the most common profile and involves a constant current applied for the stimulation period. Intermittent stimulation involves the repeated application of a constant current for several seconds followed by no stimulation. A third stimulation profile is random noise which has only been used in a single study to date (Terney et al., 2008). In this profile, a random current level between predetermined minimum and maximum values is generated several hundred times per second (Terney et al., 2008).
Direct current stimulation, known as tDCS, has been previously investigated for enhancement of working memory (for review see Utz et al., 2010). Fregni et al. (2005) applied 1 mA of anodal or cathodal tDCS to the left DLPFC healthy participants for a period of 10 min over two sessions. Participants performed with significantly better accuracy on a WM task (n-back) during anodal tDCS stimulation compared to either a sham condition or cathodal stimulation. The effects of tDCS, however, have been shown in the motor cortex to last up to an hour after the end of stimulation (Nitsche et al., 2008), which is same period of time used between conditions potentially confounding the results. Ohn et al. (2008) found that 1 mA anodal tDCS produced WM effects after 20 and 30 min of stimulation which persisted 30 min following the end of the train, suggesting some persistence of effects following DLPFC stimulation although perhaps not to the same extent as that seen in the motor cortex. Most recently Zaehele et al. (2011) found that 15 min of 1 mA anodal tDCS to the left DLPFC, compared with both sham and cathodal tDCS, resulted in significantly greater WM performance on the 2-back in healthy controls.
All of these studies used continuous tDCS: to date the effects on WM of other current profiles such as random noise have not been explored. The effects of transcranial random noise stimulation (tRNS) on motor cortex excitability were demonstrated by Terney et al. (2008) who applied tRNS between −500 and +500 μA to the left motor cortex of 17 healthy participants at a rate of 1280 samples/s for 10 min duration. Compared to the sham condition, motor cortex excitability, as revealed by transcranial magnetic stimulation (TMS), was found to increase by 20–50% during tRNS as was motor response times as measured by the serial reaction time task (SRTT) and was found to last for up to an hour after the cessation of stimulation. These findings suggest tRNS may be a promising stimulation profile for enhancement of cognitive function, however this has not been addressed to date.
Therefore, the present study aimed to assess the effect of prefrontal tRNS on WM. We compared this to sham stimulation and to the effects of an active comparator, i.e. anodal tDCS. We hypothesised that participants would demonstrate improved n-back performance following tRNS as well as following anodal tDCS compared to sham stimulation.
Section snippets
Participants
Twelve healthy participants were recruited for the study through advertisements at the Alfred Hospital in Melbourne. One participant was excluded in accordance with the exclusion criteria and 1 did not complete all testing sessions due to time constraints. The remaining 10 participants all provided informed consent and met the inclusion criteria for tDCS. Exclusion criteria were pregnancy, metal present in the head, previous head injury, any neurological condition, or any other serious medical
Outcome measures
Three tasks shown to have minimal practice effect were selected from the computer based CogState Research Version 5 suite of cognitive tasks: the one card learning task, the 1-back working memory task and the 2-back working memory task. The one card learning task presents a series of single playing cards to the participant asking each time if that card had appeared before in the task. The 1- and 2-back working memory tasks present a series of single playing cards to the participant, each time
One card learning – CogState
The results did not reveal any significant main effect of session or time for accuracy or speed on the one card learning task. Table 2 provides the means and standard deviations pre and post stimulation across all sessions for both accuracy and speed measures. The p values for the interaction effects are also provided (See Table 2).
One back working memory – CogState
There were no significant main effects of session or time for accuracy or speed on the 1-back task. Table 2 provides the means and standard deviations pre and post
Discussion
This study investigated the effect of DLPFC tRNS and anodal tDCS upon WM when applied concurrently with a task engaging WM. Performance of WM tasks after tRNS were compared to performance after both the anodal tDCS and sham conditions, allowing the anodal tDCS condition to act as an active control group. Accuracy and the speed of performance were assessed on three measures, the one card learning task and the 1-back and 2-back WM tasks. The application of tRNS resulted in no significant change
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2022, NeuroImageCitation Excerpt :With respect to our hypothesised regions of interest, tDCS has been shown to produce significant behavioural alternations in the DLPFC and cerebellum. Studies examining DLPFC stimulation have predominantly reported altered working memory performance (Mulquiney, Hoy, Daskalakis & Fitzgerald, 2011), alertness (Nelson, McKinley, Golob Warm & Parasuraman, 2014) and various cognitive tasks (see Dedoncker, Brunoni, Baeken, & Vanderhasselt, 2016 for a review); there have also been reports of effects on cognitive control (Metuki, Sela & Lavidor, 2012) and motivational states (Fregni et al., 2008). Studies of the effect of tDCS on the cerebellum have predominantly reported changes in motor function and motor learning, but there is emerging evidence for its influence on language and higher cognitive functions (Grimaldi et al., 2014; D'Mello et al., 2017).
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