BACKGROUND
tdcs has become increasingly popular for applications in clinical and neurocognitive research, with a broad range of effects and effect sizes.
tdcs has shown promise for the treatment of depression
<cit>  and stroke
<cit> , and has been documented to produce cognitive enhancement in healthy subjects in a large number of recent studies: tdcs has been shown to facilitate working memory
<cit> , motor learning
<cit> , simple somatosensory and visual motion perception learning
<cit> , and memory for word lists
<cit> .
we have previously found that tdcs can increase learning in a complex visual search task involving detection of target objects hidden in a complex virtual environment that indicate possible threats
<cit> .
in these studies, participants were trained to classify those images as target object present or target object absent.
participants received anodal tdcs at up to  <dig>  ma using 11 cm <dig> electrodes during training with the electrode positioned over 10– <dig> eeg position f <dig> .
though no differences were present at baseline in these studies, large improvements in performance occurred for participants receiving  <dig>  ma tdcs.
similar to results presented by iyer et al.
<cit> , these effects were dose-dependent, with performance improvement showing a highly linear relationship with current strength.
it is unclear from our previous studies what, specifically, mediates the effects of tdcs on learning and performance of this task.
we have found that a combined measure of glutamate and glutamine , and also n-acetyl aspartate  are all increased by tdcs under the anodal electrode, but not in the opposite hemisphere
<cit> , which may result in increased neural activity and plasticity, resulting in greater learning.
however, another possibility is that tdcs alters functioning in attentional/perceptual networks in such a way as to enhance the perception of targets, leading to greater learning by virtue of greater perceptual acuity.
the specific attentional processes that may be involved in this affect are uncertain.
here we collected three measures of attention using the attention networks test
<cit>  in effort to identify the extent to which attention is modified by tdcs over the right inferior frontal cortex.
these data were collected along with performance measures on the target learning task reported previously by our lab
<cit> .
the ant is a combination of the cued reaction time  task
<cit>  and the flanker task
<cit> , and it requires participants to indicate with a speeded button press response whether a centrally presented arrow points to the left or to the right.
efficiency of three attention networks are assessed by measuring how rt is influenced by alerting cues , spatial cues , and flankers .
these three measures have been validated in previous behavioral and imaging studies and represent functionally and anatomically distinct attention networks in the brain
<cit> .
alerting is defined as achieving and maintaining an alert state and has been linked to right hemisphere fronto-parietal brain networks
<cit> ; orienting measures the efficiency of information selection from sensory input and is mediated mainly by superior parietal cortices and frontal eye fields
<cit> ; and executive control, a measure of conflict resolution among conflicting visual stimuli, is mediated by medial and lateral frontal cortex
<cit> .
we hypothesized that measures of alerting, orienting, and/or executive attention would be enhanced with tdcs, and that increased attention in this/these enhanced domain of attention would be positively correlated with object detection scores in participants receiving active  but not sham  tdcs.
RESULTS
there were no significant differences between tdcs groups in age, years of education, gender, ratio of hours slept prior to experimentation to hours normally slept, hours spent per day playing video/computer games, or number of coffee drinkers .
tdcs significantly affected participant’s alerting attention  =  <dig> ; p =  <dig> ), with greater alerting reaction time  difference scores for participants receiving  <dig>  ma  than those receiving  <dig>  ma .
the variance in alerting rt scores for participants receiving  <dig>  ma was not significantly different from participants receiving  <dig>  ma, as determined by levene’s test for equality of variances  =  <dig> ; p =  <dig> ), suggesting that there was no significant effect of tdcs on variance of response times.
there was no statistically significant effect of tdcs on orienting or executive attention .
further analyses indicated that, for participants receiving  <dig>  ma tdcs, alerting scores were significantly correlated with the proportion of hits in the immediate test  and the delayed test , but were not correlated with hits at baseline .
none of these measures were correlated with alerting for participants receiving  <dig>  ma tdcs.
the proportion of false alarms, d’, and β were not correlated with alerting in either tdcs group .
there was a significant difference in reported skin sensation during tdcs between tdcs groups for the self-reported measure of heat  = − <dig> ; p =  <dig> ), but the difference was small and no participant receiving  <dig>  ma tdcs reported heat sensation above the minimum possible score , leading to a lack of variance within that group .
itching and tingling were not significantly different between groups and no measure of skin sensation was correlated with any measure of attention .
no measure of mood collected at the end of the experiment was significantly different between tdcs groups and mood measures were not correlated with any measure of attention .
discussion
as we have previously reported,  <dig>  ma of anodal tdcs over right inferior frontal cortex significantly increased performance with training of a difficult hidden object detection task.
in addition, we found that higher tdcs current was associated with increased measures of alerting attention.
furthermore, the proportion of hits was strongly and significantly correlated with attention scores for participants receiving  <dig>  ma tdcs.
this suggests that tdcs enhancement of object detection performance is in part related to enhancement of alerting measures of attention.
one possibility is that enhancement of alerting attention by tdcs led directly to an increased ability to detect objects in the immediate and delayed tests.
a heightened state of alertness during testing would be expected to enhance participants’ ability to identify threatening objects hidden within the complex scenes that were used in this task.
in this study we targeted the right inferior frontal cortex, a prominent node of the fronto-parietal attention network thought to support alerting attention as measured by the ant.
enhancement of alerting attention means that,  after  <dig>  ma tdcs, participants were quicker to respond to the cue stimulus within the 100 ms interval between cue and target onsets, resulting in a faster response to target stimuli, when compared with  <dig>  ma controls, or  participants receiving  <dig>  ma tdcs were able to achieve a heightened state of alertness overall, with greater priming of target perception and/or response.
enhancement of object detection could be explained to some degree by either or both of these interpretations of these results.
if participants are faster to achieve a state of cue-induced alertness, then they might have more time to search for threat stimuli in the test images.
this is unlikely to have led to the large increases in learning present in this study, however, as participants were given 2 seconds to view the images, and differences in alerting reaction time scores were on the order of 20 ms, or 1/ <dig> of the stimulus duration in the object detection task.
alternatively, a continuously heightened state of alertness could speed processing of stimuli within the complex virtual environment in this task, leading to the ability to process a greater number of objects in the image and/or more time to consider the response to the image before the end of the response window.
another possible explanation for these results is modulation of perception.
perhaps tdcs enhanced perception for both the object detection task and the ant, leading to greater performance on both measures.
if this were the case, however, one might expect that orienting and executive attention would differ between tdcs groups.
further research is needed to disentangle these possible cognitive effects of tdcs over right inferior frontal cortex.
the frontal-parietal attention network assessed by the alerting measure of the ant has been proposed by coull et al.
<cit>  to be associated with vigilance in continuous performance tasks and has been specifically implicated in sustained attention during object selection
<cit> .
tdcs may have prolonged sustained attention in this study, leading both to greater hit rate and alerting reaction time scores on the ant task.
given that the immediate test and ant were performed after approximately  <dig>  hours of experimentation, it is possible that the differences here can be explained in part by differences in the fatigue between the groups receiving  <dig>  ma and  <dig>  ma tdcs.
however, we did not find that the self-reported measure of fatigue assessed by our mood/state questionnaire was related to enhancement of alerting or that it differed between tdcs groups.
future studies might benefit from examining the relationship between tdcs of the right inferior frontal cortex and sustained attention more directly, using other attention tasks aside from the ant.
interestingly, no correlation was found between the alerting attention measure of the ant and false alarm rate or d’.
our previous studies
<cit>  have shown that tdcs significantly reduces false alarm rate and increases d’.
it is likely that the results of these previous studies can be explained by tdcs effects on multiple cognitive domains, each of which may account for effects on different performance measures for this task.
d’ is calculated by taking the difference between normalized hit rate and normalized false alarm rate.
when considered here, this suggests that the nonsignificant relationship between alerting and d’ might be explained by a nonsignificant relationship between alerting and false alarm rate specifically.
perhaps tdcs enhancement of learning and memory during training led to a greater understanding of object identities and general rules of object locations, increasing participants’ d’ scores and decreasing false alarms, while enhancement of alerting led to greater achievement and maintenance of visual search performance during the object detection task, but did not improve the false alarm rate.
another possibility is that effects of tdcs on false alarm rate result from increased risk aversion.
fecteau et al.
<cit>  show that anodal tdcs near the region targeted in this study decreases risky behavior in the balloon analog risk task , despite incentive for risky behavior.
in this context, more risk-averse participants might be more cautious in responding to ambiguous stimuli.
this would lead to a lower proportion of object-present responses in trails where no object was detected by the participant.
the ant has previously been used to examine the relationship between attention and various psychiatric and neurological disorders, including borderline personality disorder
<cit> , dyslexia
<cit> , schizophrenia
<cit> , attention-deficit hyperactivity disorder
<cit> , and depression
<cit> .
deficits in alerting as measured by the ant have been found for elderly individuals relative to a younger population
<cit> , and alerting scores have been found to vary by subtype of adhd
<cit> .
perhaps enhancement of alerting through modulation of the fronto-parietal alerting network with tdcs might reduce deficits found in these populations.
research into the application of tdcs to these clinical issues could lead to new treatments and interventions without the necessity of pharmacological therapy.
caveats
while this study demonstrates compelling evidence of tdcs effects on basic measures of attention, there were several limitations which should be mentioned.
we did not collect baseline alerting scores in this study and it is possible that differences demonstrated between participants receiving  <dig>  and  <dig>  ma tdcs were due to pre-existing differences in alerting.
this is unlikely, however, as there was no correlation between alerting scores and measures of performance on the object detection test performed before training began, and there was no difference in object detection at baseline.
also, the design of this experiment was chosen to maximize the effects on object detection performance by placing the anodal electrode over right inferior frontal cortex, but future studies examining the effects of tdcs on measures of attention obtained using the ant might benefit from using multiple electrode configurations, targeting multiple nodes implicated in the different attention networks proposed by posner and peterson
<cit> .
CONCLUSIONS
transcranial direct current stimulation directed at the right inferior frontal cortex led to a significant increase in alerting attention in this study.
this result is important both to the neuroscience community, as it demonstrates the role of this brain area in the alerting network, as proposed by posner and peterson
<cit> , and clinically, as alerting deficits are characteristic of a various neurocognitive disorders.
additionally, this effect was strongly correlated with our previously reported effects of tdcs on object detection.
these results suggest that the effects of tdcs on alerting are related to effects of tdcs on hit rate after training, but not on false alarm rate or d’.
enhancement of alternative cognitive mechanisms, such as increased neuronal plasticity during training or decreased impulsivity in responding during test, may account for the effects of tdcs on false alarm rate and d’.

 tdcs has become increasingly popular for applications in clinical and neurocognitive research, with a broad range of effects and effect sizes. tdcs has shown promise for the treatment of depression and stroke, and has been documented to produce cognitive enhancement in healthy subjects in a large number of recent studies: tdcs has been shown to facilitate working memory, motor learning, simple somatosensory and visual motion perception learning, and memory for word lists. we have previously found that tdcs can increase learning in a complex visual search task involving detection of target objects hidden in a complex virtual environment that indicate possible threats. in these studies, participants were trained to classify those images as target object present or target object absent. participants received anodal tdcs at up to  ma using 11 cm electrodes during training with the electrode positioned over 10– eeg position f. though no differences were present at baseline in these studies, large improvements in performance occurred for participants receiving  ma tdcs. similar to results presented by iyer et al., these effects were dose-dependent, with performance improvement showing a highly linear relationship with current strength. it is unclear from our previous studies what, specifically, mediates the effects of tdcs on learning and performance of this task. we have found that a combined measure of glutamate and glutamine, and also n-acetyl aspartate are all increased by tdcs under the anodal electrode, but not in the opposite hemisphere, which may result in increased neural activity and plasticity, resulting in greater learning. however, another possibility is that tdcs alters functioning in attentional/perceptual networks in such a way as to enhance the perception of targets, leading to greater learning by virtue of greater perceptual acuity. the specific attentional processes that may be involved in this affect are uncertain. here we collected three measures of attention using the attention networks test in effort to identify the extent to which attention is modified by tdcs over the right inferior frontal cortex. these data were collected along with performance measures on the target learning task reported previously by our lab. the ant is a combination of the cued reaction time task and the flanker task, and it requires participants to indicate with a speeded button press response whether a centrally presented arrow points to the left or to the right. efficiency of three attention networks are assessed by measuring how rt is influenced by alerting cues, spatial cues, and flankers. these three measures have been validated in previous behavioral and imaging studies and represent functionally and anatomically distinct attention networks in the brain. alerting is defined as achieving and maintaining an alert state and has been linked to right hemisphere fronto-parietal brain networks; orienting measures the efficiency of information selection from sensory input and is mediated mainly by superior parietal cortices and frontal eye fields; and executive control, a measure of conflict resolution among conflicting visual stimuli, is mediated by medial and lateral frontal cortex. we hypothesized that measures of alerting, orienting, and/or executive attention would be enhanced with tdcs, and that increased attention in this/these enhanced domain of attention would be positively correlated with object detection scores in participants receiving active but not sham tdcs.  there were no significant differences between tdcs groups in age, years of education, gender, ratio of hours slept prior to experimentation to hours normally slept, hours spent per day playing video/computer games, or number of coffee drinkers. tdcs significantly affected participant’s alerting attention  = ; p =  ), with greater alerting reaction time difference scores for participants receiving  ma than those receiving  ma. the variance in alerting rt scores for participants receiving  ma was not significantly different from participants receiving  ma, as determined by levene’s test for equality of variances  = ; p =  ), suggesting that there was no significant effect of tdcs on variance of response times. there was no statistically significant effect of tdcs on orienting or executive attention. further analyses indicated that, for participants receiving  ma tdcs, alerting scores were significantly correlated with the proportion of hits in the immediate test and the delayed test, but were not correlated with hits at baseline. none of these measures were correlated with alerting for participants receiving  ma tdcs. the proportion of false alarms, d’, and β were not correlated with alerting in either tdcs group. there was a significant difference in reported skin sensation during tdcs between tdcs groups for the self-reported measure of heat  = −; p =  ), but the difference was small and no participant receiving  ma tdcs reported heat sensation above the minimum possible score, leading to a lack of variance within that group. itching and tingling were not significantly different between groups and no measure of skin sensation was correlated with any measure of attention. no measure of mood collected at the end of the experiment was significantly different between tdcs groups and mood measures were not correlated with any measure of attention. discussion as we have previously reported,  ma of anodal tdcs over right inferior frontal cortex significantly increased performance with training of a difficult hidden object detection task. in addition, we found that higher tdcs current was associated with increased measures of alerting attention. furthermore, the proportion of hits was strongly and significantly correlated with attention scores for participants receiving  ma tdcs. this suggests that tdcs enhancement of object detection performance is in part related to enhancement of alerting measures of attention. one possibility is that enhancement of alerting attention by tdcs led directly to an increased ability to detect objects in the immediate and delayed tests. a heightened state of alertness during testing would be expected to enhance participants’ ability to identify threatening objects hidden within the complex scenes that were used in this task. in this study we targeted the right inferior frontal cortex, a prominent node of the fronto-parietal attention network thought to support alerting attention as measured by the ant. enhancement of alerting attention means that, after  ma tdcs, participants were quicker to respond to the cue stimulus within the 100 ms interval between cue and target onsets, resulting in a faster response to target stimuli, when compared with  ma controls, or participants receiving  ma tdcs were able to achieve a heightened state of alertness overall, with greater priming of target perception and/or response. enhancement of object detection could be explained to some degree by either or both of these interpretations of these results. if participants are faster to achieve a state of cue-induced alertness, then they might have more time to search for threat stimuli in the test images. this is unlikely to have led to the large increases in learning present in this study, however, as participants were given 2 seconds to view the images, and differences in alerting reaction time scores were on the order of 20 ms, or 1/ of the stimulus duration in the object detection task. alternatively, a continuously heightened state of alertness could speed processing of stimuli within the complex virtual environment in this task, leading to the ability to process a greater number of objects in the image and/or more time to consider the response to the image before the end of the response window. another possible explanation for these results is modulation of perception. perhaps tdcs enhanced perception for both the object detection task and the ant, leading to greater performance on both measures. if this were the case, however, one might expect that orienting and executive attention would differ between tdcs groups. further research is needed to disentangle these possible cognitive effects of tdcs over right inferior frontal cortex. the frontal-parietal attention network assessed by the alerting measure of the ant has been proposed by coull et al. to be associated with vigilance in continuous performance tasks and has been specifically implicated in sustained attention during object selection. tdcs may have prolonged sustained attention in this study, leading both to greater hit rate and alerting reaction time scores on the ant task. given that the immediate test and ant were performed after approximately  hours of experimentation, it is possible that the differences here can be explained in part by differences in the fatigue between the groups receiving  ma and  ma tdcs. however, we did not find that the self-reported measure of fatigue assessed by our mood/state questionnaire was related to enhancement of alerting or that it differed between tdcs groups. future studies might benefit from examining the relationship between tdcs of the right inferior frontal cortex and sustained attention more directly, using other attention tasks aside from the ant. interestingly, no correlation was found between the alerting attention measure of the ant and false alarm rate or d’. our previous studies have shown that tdcs significantly reduces false alarm rate and increases d’. it is likely that the results of these previous studies can be explained by tdcs effects on multiple cognitive domains, each of which may account for effects on different performance measures for this task. d’ is calculated by taking the difference between normalized hit rate and normalized false alarm rate. when considered here, this suggests that the nonsignificant relationship between alerting and d’ might be explained by a nonsignificant relationship between alerting and false alarm rate specifically. perhaps tdcs enhancement of learning and memory during training led to a greater understanding of object identities and general rules of object locations, increasing participants’ d’ scores and decreasing false alarms, while enhancement of alerting led to greater achievement and maintenance of visual search performance during the object detection task, but did not improve the false alarm rate. another possibility is that effects of tdcs on false alarm rate result from increased risk aversion. fecteau et al. show that anodal tdcs near the region targeted in this study decreases risky behavior in the balloon analog risk task, despite incentive for risky behavior. in this context, more risk-averse participants might be more cautious in responding to ambiguous stimuli. this would lead to a lower proportion of object-present responses in trails where no object was detected by the participant. the ant has previously been used to examine the relationship between attention and various psychiatric and neurological disorders, including borderline personality disorder, dyslexia, schizophrenia, attention-deficit hyperactivity disorder, and depression. deficits in alerting as measured by the ant have been found for elderly individuals relative to a younger population, and alerting scores have been found to vary by subtype of adhd. perhaps enhancement of alerting through modulation of the fronto-parietal alerting network with tdcs might reduce deficits found in these populations. research into the application of tdcs to these clinical issues could lead to new treatments and interventions without the necessity of pharmacological therapy. caveats while this study demonstrates compelling evidence of tdcs effects on basic measures of attention, there were several limitations which should be mentioned. we did not collect baseline alerting scores in this study and it is possible that differences demonstrated between participants receiving and  ma tdcs were due to pre-existing differences in alerting. this is unlikely, however, as there was no correlation between alerting scores and measures of performance on the object detection test performed before training began, and there was no difference in object detection at baseline. also, the design of this experiment was chosen to maximize the effects on object detection performance by placing the anodal electrode over right inferior frontal cortex, but future studies examining the effects of tdcs on measures of attention obtained using the ant might benefit from using multiple electrode configurations, targeting multiple nodes implicated in the different attention networks proposed by posner and peterson.  transcranial direct current stimulation directed at the right inferior frontal cortex led to a significant increase in alerting attention in this study. this result is important both to the neuroscience community, as it demonstrates the role of this brain area in the alerting network, as proposed by posner and peterson, and clinically, as alerting deficits are characteristic of a various neurocognitive disorders. additionally, this effect was strongly correlated with our previously reported effects of tdcs on object detection. these results suggest that the effects of tdcs on alerting are related to effects of tdcs on hit rate after training, but not on false alarm rate or d’. enhancement of alternative cognitive mechanisms, such as increased neuronal plasticity during training or decreased impulsivity in responding during test, may account for the effects of tdcs on false alarm rate and d’. 
we previously found that transcranial direct current stimulation improves learning and performance in a task where subjects learn to detect potential threats indicated by small target objects hidden in a complex virtual environment. these results indicate that tdcs enhancement of performance in this task may be related in part to the enhancement of alerting attention, which may benefit the initial identification, learning and/or subsequent recognition of target objects indicating potential threats. alerting, but not orienting or executive attention, was significantly higher for participants receiving  ma compared with  ma tdcs.
 we previously found that transcranial direct current stimulation improves learning and performance in a task where subjects learn to detect potential threats indicated by small target objects hidden in a complex virtual environment. in the present study, we examined the hypothesis that these effects on learning and performance are related to changes in attention. the effects of tdcs were tested for three forms of attention using the attention network task, which were compared with performance on the object-learning task.  participants received either  ma or  ma tdcs during training and were tested for performance in object-identification before training and again immediately after training. participants next performed the attention networks task, and were later tested for object-identification performance a final time. alerting, but not orienting or executive attention, was significantly higher for participants receiving  ma compared with  ma tdcs. furthermore, alerting scores were significantly correlated with the proportion of hits for participants receiving  ma.  these results indicate that tdcs enhancement of performance in this task may be related in part to the enhancement of alerting attention, which may benefit the initial identification, learning and/or subsequent recognition of target objects indicating potential threats. learningtdcsfrontal cortexobject detectionvisual searchbrain stimulationattentionalertingattention networks test 