Bruce D. McCandliss

Testing the Efficiency and Independence of Attentional Networks

In recent years, three attentional networks have been defined in anatomical and functional terms. These functions involve alerting, orienting, and executive attention. Reaction time measures can be used to quantify the processing efficiency within each of these three networks. The Attention Network Test (ANT) is designed to evaluate alerting, orienting, and executive attention within a single 30-min testing session that can be easily performed by children, patients, and monkeys. A study with 40 normal adult subjects indicates that the ANT produces reliable single subject estimates of alerting, orienting, and executive function, and further suggests that the efficiencies of these three networks are uncorrelated. There are, however, some interactions in which alerting and orienting can modulate the degree of interference from flankers. This procedure may prove to be convenient and useful in evaluating attentional abnormalities associated with cases of brain injury, stroke, schizophrenia, and attention-deficit disorder. The ANT may also serve as an activation task for neuroimaging studies and as a phenotype for the study of the influence of genes on attentional networks.

The activation of attentional networks

Alerting, orienting, and executive control are widely thought to be relatively independent aspects of attention that are linked to separable brain regions. However, neuroimaging studies have yet to examine evidence for the anatomical separability of these three aspects of attention in the same subjects performing the same task. The attention network test (ANT) examines the effects of cues and targets within a single reaction time task to provide a means of exploring the efficiency of the alerting, orienting, and executive control networks involved in attention. It also provides an opportunity to examine the brain activity of these three networks as they operate in a single integrated task. We used event-related functional magnetic resonance imaging (fMRI) to explore the brain areas involved in the three attention systems targeted by the ANT. The alerting contrast showed strong thalamic involvement and activation of anterior and posterior cortical sites. As expected, the orienting contrast activated parietal sites and frontal eye fields. The executive control network contrast showed activation of the anterior cingulate along with several other brain areas. With some exceptions, activation patterns of these three networks within this single task are consistent with previous fMRI studies that have been studied in separate tasks. Overall, the fMRI results suggest that the functional contrasts within this single task differentially activate three separable anatomical networks related to the components of attention.

The visual word form area: expertise for reading in the fusiform gyrus

Brain imaging studies reliably localize a region of visual cortex that is especially responsive to visual words. This brain specialization is essential to rapid reading ability because it enhances perception of words by becoming specifically tuned to recurring properties of a writing system. The origin of this specialization poses a challenge for evolutionary accounts involving innate mechanisms for functional brain organization. We propose an alternative account, based on studies of other forms of visual expertise (i.e. bird and car experts) that lead to functional reorganization. We argue that the interplay between the unique demands of word reading and the structural constraints of the visual system lead to the emergence of the Visual Word Form Area.

Development of attentional networks in childhood

Recent research in attention has involved three networks of anatomical areas that carry out the functions of orienting, alerting and executive control (including conflict monitoring). There have been extensive cognitive and neuroimaging studies of these networks in adults. We developed an integrated Attention Network Test (ANT) to measure the efficiency of the three networks with adults. We have now adapted this test to study the development of these networks during childhood. The test is a child-friendly version of the flanker task with alerting and orienting cues. We studied the development of the attentional networks in a cross-sectional experiment with four age groups ranging from 6 through 9 (Experiment 1). In a second experiment, we compared children (age 10 years) and adult performance in both child and adults versions of the ANT. Reaction time and accuracy improved at each age interval and positive values were found for the average efficiency of each of the networks. Alertness showed evidence of change up to and beyond age 10, while conflict scores appear stable after age seven and orienting scores do not change in the age range studied. A final experiment with forty 7-year-old children suggested that children like adults showed independence between the three networks under some conditions.

Cognitive and brain consequences of conflict

Tasks involving conflict between stimulus dimensions have been shown to activate dorsal anterior cingulate and prefrontal areas. It has been proposed that the dorsal anterior cingulate is involved a domain general process of monitoring conflict, while prefrontal areas are involved in resolving conflict. We examine three tasks that all require people to respond based on one stimulus dimension while ignoring another conflicting dimension, but which vary in the source of conflict. One of the tasks uses language stimuli (Stroop effect) and two use nonlanguage spatial conflicts appropriate for children and nonhuman animals. In Experiment 1, 12 participants were studied with event-related functional magnetic resonance imaging (fMRI) while performing each of the three tasks. Reaction times for each of the three tasks were significantly longer in the incongruent condition compared with the congruent condition, demonstrating that each task elicits a conflict. By studying the same people in the same session, we test the hypothesis that conflict activates a similar brain network in the three tasks. Significant activations were found in the anterior cingulate and left prefrontal cortex for all three conflict tasks. Within these regions, the conflict component demonstrated evidence for significant common activation across the three tasks, although the peak activation point and spatial extent were not identical. Other areas demonstrated activation unique to each task. Experiments 2-4 provide behavioral evidence indicating considerable independence between conflict operations involved in the tasks. The behavioral and fMRI results taken together seem to argue against a single unified network for processing conflict, but instead support either distinct networks for each conflict task or a single network that monitors conflict with different sites used to resolve the conflict.

Extent of Microstructural White Matter Injury in Postconcussive Syndrome Correlates with Impaired Cognitive Reaction Time: A 3T Diffusion Tensor Imaging Study of Mild Traumatic Brain Injury

BACKGROUND AND PURPOSE: Diffusion tensor imaging (DTI) may be a useful index of microstructural changes implicated in diffuse axonal injury (DAI) linked to persistent postconcussive symptoms, especially in mild traumatic brain injury (TBI), for which conventional MR imaging techniques may lack sensitivity. We hypothesized that for mild TBI, DTI measures of DAI would correlate with impairments in reaction time, whereas the number of focal lesions on conventional 3T MR imaging would not. MATERIALS AND METHODS: Thirty-four adult patients with mild TBI with persistent symptoms were assessed for DAI by quantifying traumatic microhemorrhages detected on a conventional set of T2*-weighted gradient-echo images and by DTI measures of fractional anisotropy (FA) within a set of a priori regions of interest. FA values 2.5 SDs below the region average, based on a group of 26 healthy control adults, were coded as exhibiting DAI. RESULTS: DTI measures revealed several predominant regions of damage including the anterior corona radiata (41% of the patients), uncinate fasciculus (29%), genu of the corpus callosum (21%), inferior longitudinal fasciculus (21%), and cingulum bundle (18%). The number of damaged white matter structures as quantified by DTI was significantly correlated with mean reaction time on a simple cognitive task (r = 0.49, P = .012). In contradistinction, the number of traumatic microhemorrhages was uncorrelated with reaction time (r = −0.08, P = .71). CONCLUSION: Microstructural white matter lesions detected by DTI correlate with persistent cognitive deficits in mild TBI, even in populations in which conventional measures do not. DTI measures may thus contribute additional diagnostic information related to DAI.

Possible axonal regrowth in late recovery from the minimally conscious state

We used diffusion tensor imaging (DTI) to study 2 patients with traumatic brain injury. The first patient recovered reliable expressive language after 19 years in a minimally conscious state (MCS); the second had remained in MCS for 6 years. Comparison of white matter integrity in the patients and 20 normal subjects using histograms of apparent diffusion constants and diffusion anisotropy identified widespread altered diffusivity and decreased anisotropy in the damaged white matter. These findings remained unchanged over an 18-month interval between 2 studies in the first patient. In addition, in this patient, we identified large, bilateral regions of posterior white matter with significantly increased anisotropy that reduced over 18 months. In contrast, notable increases in anisotropy within the midline cerebellar white matter in the second study correlated with marked clinical improvements in motor functions. This finding was further correlated with an increase in resting metabolism measured by PET in this subregion. Aberrant white matter structures were evident in the second patients DTI images but were not clinically correlated. We propose that axonal regrowth may underlie these findings and provide a biological mechanism for late recovery. Our results are discussed in the context of recent experimental studies that support this inference.

The face-specific N170 component is modulated by emotional facial expression.

BackgroundAccording to the traditional two-stage model of face processing, the face-specific N170 event-related potential (ERP) is linked to structural encoding of face stimuli, whereas later ERP components are thought to reflect processing of facial affect. This view has recently been challenged by reports of N170 modulations by emotional facial expression. This study examines the time-course and topography of the influence of emotional expression on the N170 response to faces.MethodsDense-array ERPs were recorded in response to a set (n = 16) of fear and neutral faces. Stimuli were normalized on dimensions of shape, size and luminance contrast distribution. To minimize task effects related to facial or emotional processing, facial stimuli were irrelevant to a primary task of learning associative pairings between a subsequently presented visual character and a spoken word.ResultsN170 to faces showed a strong modulation by emotional facial expression. A split half analysis demonstrates that this effect was significant both early and late in the experiment and was therefore not associated with only the initial exposures of these stimuli, demonstrating a form of robustness against habituation. The effect of emotional modulation of the N170 to faces did not show significant interaction with the gender of the face stimulus, or hemisphere of recording sites. Subtracting the fear versus neutral topography provided a topography that itself was highly similar to the face N170.ConclusionThe face N170 response can be influenced by emotional expressions contained within facial stimuli. The topography of this effect is consistent with the notion that fear stimuli exaggerates the N170 response itself. This finding stands in contrast to previous models suggesting that N170 processes linked to structural analysis of faces precede analysis of emotional expression, and instead may reflect early top-down modulation from neural systems involved in rapid emotional processing.

Neural systems predicting long-term outcome in dyslexia

Individuals with developmental dyslexia vary in their ability to improve reading skills, but the brain basis for improvement remains largely unknown. We performed a prospective, longitudinal study over 2.5 y in children with dyslexia (n = 25) or without dyslexia (n = 20) to discover whether initial behavioral or brain measures, including functional MRI (fMRI) and diffusion tensor imaging (DTI), can predict future long-term reading gains in dyslexia. No behavioral measure, including widely used and standardized reading and language tests, reliably predicted future reading gains in dyslexia. Greater right prefrontal activation during a reading task that demanded phonological awareness and right superior longitudinal fasciculus (including arcuate fasciculus) white-matter organization significantly predicted future reading gains in dyslexia. Multivariate pattern analysis (MVPA) of these two brain measures, using linear support vector machine (SVM) and cross-validation, predicted significantly above chance (72% accuracy) which particular child would or would not improve reading skills (behavioral measures were at chance). MVPA of whole-brain activation pattern during phonological processing predicted which children with dyslexia would improve reading skills 2.5 y later with >90% accuracy. These findings identify right prefrontal brain mechanisms that may be critical for reading improvement in dyslexia and that may differ from typical reading development. Brain measures that predict future behavioral outcomes (neuroprognosis) may be more accurate, in some cases, than available behavioral measures.

The relation of brain oscillations to attentional networks

Previous studies have suggested the relation of particular frequency bands such as theta (4–8 Hz), alpha (8–14 Hz), beta (14–30 Hz), or gamma (>30 Hz) to cognitive functions. However, there has been controversy over which bands are specifically related to attention. We used the attention network test to separate three anatomically defined brain networks that carry out the functions of alerting, orienting, and executive control of attention. High-density scalp electrical recording was performed to record synchronous oscillatory activity and power spectrum analyses based on functional magnetic resonance imaging constrained dipole modeling were conducted for each attentional network. We found that each attentional network has a distinct set of oscillations related to its activity. The alerting network showed a specific decrease in theta-, alpha-, and beta-band activity 200–450 ms after a warning signal. The orienting network showed an increase in gamma-band activity at ∼200 ms after a spatial cue, indicating the location of a target. The executive control network revealed a complex pattern when a target was surrounded with incongruent flankers compared with congruent flankers. There was an early (<400 ms) increase in gamma-band activity, a later (>400 ms) decrease in beta- and low gamma-band activity after the target onset, and a decrease of all frequency bands before response followed by an increase after the response. These data demonstrate that attention is not related to any single frequency band but that each network has a distinct oscillatory activity and time course.