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1.
Nat Hum Behav ; 4(8): 844-855, 2020 08.
Article in English | MEDLINE | ID: mdl-32313233

ABSTRACT

Animal neurophysiological studies have identified neural signals within dorsal frontoparietal areas that trace a perceptual decision by accumulating sensory evidence over time and trigger action upon reaching a threshold. Although analogous accumulation-to-bound signals are identifiable on extracranial human electroencephalography, their cortical origins remain unknown. Here neural metrics of human evidence accumulation, predictive of the speed of perceptual reports, were isolated using electroencephalography and related to dorsal frontoparietal network (dFPN) connectivity using diffusion and resting-state functional magnetic resonance imaging. The build-up rate of evidence accumulation mediated the relationship between the white matter macrostructure of dFPN pathways and the efficiency of perceptual reports. This association between steeper build-up rates of evidence accumulation and the dFPN was recapitulated in the resting-state networks. Stronger connectivity between dFPN regions is thus associated with faster evidence accumulation and speeded perceptual decisions. Our findings identify an integrated network for perceptual decisions that may be targeted for neurorehabilitation in cognitive disorders.


Subject(s)
Decision Making/physiology , Frontal Lobe/physiology , Parietal Lobe/physiology , Perception/physiology , Adolescent , Electroencephalography , Female , Frontal Lobe/diagnostic imaging , Functional Neuroimaging , Humans , Magnetic Resonance Imaging , Male , Neural Pathways/physiology , Parietal Lobe/diagnostic imaging , White Matter/diagnostic imaging , White Matter/physiology , Young Adult
2.
Elife ; 82019 03 18.
Article in English | MEDLINE | ID: mdl-30882347

ABSTRACT

The timing and accuracy of perceptual decision-making is exquisitely sensitive to fluctuations in arousal. Although extensive research has highlighted the role of various neural processing stages in forming decisions, our understanding of how arousal impacts these processes remains limited. Here we isolated electrophysiological signatures of decision-making alongside signals reflecting target selection, attentional engagement and motor output and examined their modulation as a function of tonic and phasic arousal, indexed by baseline and task-evoked pupil diameter, respectively. Reaction times were shorter on trials with lower tonic, and higher phasic arousal. Additionally, these two pupil measures were predictive of a unique set of EEG signatures that together represent multiple information processing steps of decision-making. Finally, behavioural variability associated with fluctuations in tonic and phasic arousal, indicative of neuromodulators acting on multiple timescales, was mediated by its effects on the EEG markers of attentional engagement, sensory processing and the variability in decision processing.


Subject(s)
Arousal , Decision Making , Psychomotor Performance , Pupil/physiology , Visual Perception , Attention , Electroencephalography , Humans , Locomotion
3.
J Neurosci ; 38(9): 2163-2176, 2018 02 28.
Article in English | MEDLINE | ID: mdl-29371320

ABSTRACT

Despite their small size, microsaccades can impede stimulus detections if executed at inopportune times. Although it has been shown that microsaccades evoke both inhibitory and excitatory responses across different visual regions, their impact on the higher-level neural decision processes that bridge sensory responses to action selection has yet to be examined. Here, we show that when human observers monitor stimuli for subtle feature changes, the occurrence of microsaccades long after (up to 800 ms) change onset predicts slower reaction times and this is accounted for by momentary suppression of neural signals at each key stage of decision formation: visual evidence encoding, evidence accumulation, and motor preparation. Our data further reveal that, independent of the timing of the change events, the onset of neural decision formation coincides with a systematic inhibition of microsaccade production, persisting until the perceptual report is executed. Our combined behavioral and neural measures highlight antagonistic interactions between microsaccade occurrence and evidence accumulation during visual decision-making tasks.SIGNIFICANCE STATEMENT When fixating on a location in space, we frequently make tiny eye movements called microsaccades. In the present study, we show that these microsaccades impede our ability to make perceptual decisions about visual stimuli and this impediment specifically occurs via the disruption of several processing levels of the sensorimotor network: the encoding of visual evidence itself, the accumulation of visual evidence toward a response, and effector-selective motor preparation. Furthermore, we show that the production of microsaccades is inhibited during the perceptual decision, possibly as a counteractive measure to mitigate their negative effect on behavior in this context. The combined behavioral and neural measures used in this study provide strong and novel evidence for the interaction of fixational eye movements and the perceptual decision-making process.


Subject(s)
Decision Making/physiology , Saccades/physiology , Visual Perception/physiology , Adult , Female , Humans , Male , Reaction Time/physiology
4.
J Neurosci ; 37(12): 3378-3385, 2017 03 22.
Article in English | MEDLINE | ID: mdl-28242798

ABSTRACT

Healthy subjects tend to exhibit a bias of visual attention whereby left hemifield stimuli are processed more quickly and accurately than stimuli appearing in the right hemifield. It has long been held that this phenomenon arises from the dominant role of the right cerebral hemisphere in regulating attention. However, methods that would enable more precise understanding of the mechanisms underpinning visuospatial bias have remained elusive. We sought to finely trace the temporal evolution of spatial biases by leveraging a novel bilateral dot motion detection paradigm. In combination with electroencephalography, this paradigm enables researchers to isolate discrete neural signals reflecting the key neural processes needed for making these detection decisions. These include signals for spatial attention, early target selection, evidence accumulation, and motor preparation. Using this method, we established that three key neural markers accounted for unique between-subject variation in visuospatial bias: hemispheric asymmetry in posterior α power measured before target onset, which is related to the distribution of preparatory attention across the visual field; asymmetry in the peak latency of the early N2c target-selection signal; and, finally, asymmetry in the onset time of the subsequent neural evidence-accumulation process with earlier onsets for left hemifield targets. Our development of a single paradigm to dissociate distinct processing components that track the temporal evolution of spatial biases not only advances our understanding of the neural mechanisms underpinning normal visuospatial attention bias, but may also in the future aid differential diagnoses in disorders of spatial attention.SIGNIFICANCE STATEMENT The significance of this research is twofold. First, it shows that individual differences in how humans direct their attention between left and right space reflects physiological differences in how early the brain starts to accumulate evidence for the existence of a visual target. Second, the novel methods developed here may have particular relevance to disorders of attention, such as unilateral spatial neglect. In the case of spatial neglect, pathological inattention to left space could have multiple underlying causes, including biased attention, impaired decision formation, or a motor deficit related to one side of space. Our development of a single paradigm to dissociate each of these components may aid in supporting more precise differential diagnosis in such heterogeneous disorders.


Subject(s)
Attention/physiology , Dominance, Cerebral/physiology , Reaction Time/physiology , Space Perception/physiology , Visual Fields/physiology , Visual Perception/physiology , Adolescent , Adult , Female , Humans , Male , Task Performance and Analysis , Young Adult
6.
Sci Rep ; 6: 27754, 2016 06 13.
Article in English | MEDLINE | ID: mdl-27291291

ABSTRACT

Brain networks subserving alertness in humans interact with those for spatial attention orienting. We employed blue-enriched light to directly manipulate alertness in healthy volunteers. We show for the first time that prior exposure to higher, relative to lower, intensities of blue-enriched light speeds response times to left, but not right, hemifield visual stimuli, via an asymmetric effect on right-hemisphere parieto-occipital α-power. Our data give rise to the tantalising possibility of light-based interventions for right hemisphere disorders of spatial attention.


Subject(s)
Attention/physiology , Neurons/physiology , Photic Stimulation/methods , Space Perception/physiology , Adult , Female , Fluorescence , Functional Laterality , Humans , Male , Reaction Time , Young Adult
7.
Curr Biol ; 26(4): 496-502, 2016 Feb 22.
Article in English | MEDLINE | ID: mdl-26853360

ABSTRACT

Computational and neurophysiological research has highlighted neural processes that accumulate sensory evidence for perceptual decisions. These processes have been studied in the context of highly simplified perceptual discrimination paradigms in which the physical evidence appears at times and locations that are either entirely predictable or exogenously cued (e.g., by the onset of the stimulus itself). Yet, we are rarely afforded such certainty in everyday life. For example, when driving along a busy motorway, we must continually monitor the movements of surrounding vehicles for events that call for a lane change. In such scenarios, it is unknown which of the continuously present information sources will become relevant or when. Although it is well established that evidence integration provides an effective mechanism for countering the impact of noise, the question of how this mechanism is implemented in the face of uncertain evidence onsets has yet to be answered. Here, we show that when monitoring two potential sources of information for evidence occurring unpredictably in both time and space, the human brain employs discrete, early target selection signals that significantly modulate the onset and rate of neural evidence accumulation, and thereby the timing and accuracy of perceptual reports. These selection signals share many of the key characteristics of the N2pc component highlighted in the literature on visual search yet are present even in the absence of distractors and under situations of low temporal and spatial uncertainty. These data provide novel insights into how target selection supports decision making in uncertain environments.


Subject(s)
Brain/physiology , Decision Making , Uncertainty , Visual Perception , Adolescent , Adult , Female , Humans , Male , Young Adult
8.
R Soc Open Sci ; 3(1): 150547, 2016 Jan.
Article in English | MEDLINE | ID: mdl-26909182

ABSTRACT

Openness is one of the central values of science. Open scientific practices such as sharing data, materials and analysis scripts alongside published articles have many benefits, including easier replication and extension studies, increased availability of data for theory-building and meta-analysis, and increased possibility of review and collaboration even after a paper has been published. Although modern information technology makes sharing easier than ever before, uptake of open practices had been slow. We suggest this might be in part due to a social dilemma arising from misaligned incentives and propose a specific, concrete mechanism-reviewers withholding comprehensive review-to achieve the goal of creating the expectation of open practices as a matter of scientific principle.

9.
Article in English | MEDLINE | ID: mdl-29560866

ABSTRACT

BACKGROUND: Attention-deficit/hyperactivity disorder (ADHD) is a prevalent neurodevelopmental disorder with prominent impairments in directing and sustaining attention. The aim of this study was to identify the neurophysiologic bases of attention deficits in ADHD, focusing on electroencephalography markers of attentional selection (posterior contralateral N2 [N2pc]) and suppression (distractor positivity [PD]). METHODS: The electroencephalography data were collected from 135 children 9-15 years old with and without ADHD while they searched for a shape target in either the absence (experiment 1) or the presence (experiment 2) of a salient but irrelevant color distractor. RESULTS: In experiment 1, the shape target elicited a smaller N2pc in children with ADHD (n = 38) compared with typically developing children (n = 36). The smaller N2pc amplitude predicted higher levels of inattentive symptoms in children with ADHD. Moreover, the target-elicited N2pc was followed by a positivity in typically developing children but not in children with ADHD. In experiment 2, the salient but irrelevant color distractor elicited a smaller PD component in children with ADHD (n = 32) compared with typically developing children (n = 29). The smaller PD predicted higher inattentive symptom severity as well as lower behavioral accuracy in children with ADHD. CONCLUSIONS: The correlation between N2pc/PD amplitudes and ADHD symptom severity suggests that these signals of attentional selection and suppression may serve as potential candidates for neurophysiologic markers of ADHD. Our findings provide a neurophysiologic basis for the subjective reports of attention deficits in children with ADHD and highlight the importance of spatial attention impairments in ADHD.

10.
Am J Med Genet B Neuropsychiatr Genet ; 168B(2): 89-96, 2015 Mar.
Article in English | MEDLINE | ID: mdl-25656223

ABSTRACT

Previous genetic studies have postulated that attention deficit hyperactivity disorder (ADHD) should be regarded as the extreme end of a set of behavioural traits that can be continuously measured in the general population. The current study adopted a quantitative trait approach to examine the relationship between dopamine gene variants and self-reported ADHD symptoms in 517 nonclinical adults. Although genetic associations with variants of both the dopamine transporter (DAT1; SLC6A3) and D4 receptor (DRD4) genes have been reliably reported in children, results in adults are less consistent. We probed two potentially functional variable number of tandem repeat (VNTR) polymorphisms in the 3'UTR and intron 8 of DAT1, the 10-repeat and 6-repeat alleles of which respectively form a haplotype (10/6 DAT1 haplotype) that is associated with childhood ADHD. We also genotyped the exon 3 VNTR of DRD4, the 7-repeat allele of which is also an established risk factor for childhood ADHD. Permutation analysis showed an influence of the 10/6 DAT1 haplotype on both CAARS-G and CAARS-H (DSM-IV ADHD Symptoms Total and ADHD Index respectively), such that ADHD symptom scores increased with each additional copy of the 10/6 DAT1 haplotype. This result survived corrections for multiple comparisons both at the level of genotype and phenotype. A nominal association with CAARS-G was also found for the 7-repeat allele of the DRD4 VNTR however this did not survive multiple comparison correction. Our results provide further support for the influence of variation in the 10/6 DAT1 haplotype and individual differences in ADHD symptoms in adults.


Subject(s)
Attention Deficit Disorder with Hyperactivity/genetics , Dopamine Plasma Membrane Transport Proteins/genetics , Genetic Association Studies , Genetic Predisposition to Disease , Haplotypes/genetics , Adult , Alleles , Gene Dosage , Humans , Minisatellite Repeats/genetics , Receptors, Dopamine D4/genetics , Risk Factors
11.
J Neurosci ; 34(47): 15743-50, 2014 Nov 19.
Article in English | MEDLINE | ID: mdl-25411502

ABSTRACT

Although lateral asymmetries in orienting behavior are evident across species and have been linked to interhemispheric asymmetries in dopamine signaling, the relative contribution of attentional versus motoric processes remains unclear. Here we took a cognitive genetic approach to adjudicate between roles for dopamine in attentional versus response selection. A sample of nonclinical adult humans (N = 518) performed three cognitive tasks (spatial attentional competition, spatial cueing, and flanker tasks) that varied in the degree to which they required participants to resolve attentional or response competition. All participants were genotyped for two putatively functional tandem repeat polymorphisms of the dopamine transporter gene (DAT1; SLC6A3), which are argued to influence the level of available synaptic dopamine and confer risk to disorders of inattention. DAT1 genotype modulated the task-specific effects of the various task-irrelevant stimuli across both the spatial competition and spatial cueing but not flanker tasks. Specifically, compared with individuals carrying one or two copies of the 10-repeat DAT1 allele, individuals without this allele demonstrated an immunity to distraction, such that response times were unaffected by increases in the number of distractor stimuli, particularly when these were presented predominantly in the left hemifield. All three genotype groups exhibited uniform costs of resolving leftward response selection in a standard flanker task. None of these significant effects could be explained by speed-accuracy trade-offs, suggesting that participants without the 10-repeat allele of the DAT1 tandem repeat polymorphism possess an enhanced attentional ability to suppress task-irrelevant stimuli in the left hemifield.


Subject(s)
Attention/physiology , Dopamine Plasma Membrane Transport Proteins/genetics , Cognition/physiology , Cues , Female , Functional Laterality/genetics , Functional Laterality/physiology , Genotype , Humans , Male , Orientation/physiology , Psychomotor Performance/physiology , Space Perception/physiology , Young Adult
12.
Neuropsychologia ; 64: 33-40, 2014 11.
Article in English | MEDLINE | ID: mdl-25234646

ABSTRACT

Healthy subjects typically exhibit a subtle bias of visuospatial attention favouring left space that is commonly termed 'pseudoneglect'. This bias is attenuated, or shifted rightwards, with decreasing alertness over time, consistent with theoretical models proposing that pseudoneglect is a result of the right hemisphere׳s dominance in regulating attention. Although this 'time-on-task effect' for spatial bias is observed when averaging across whole samples of healthy participants, Benwell, C. S. Y., Thut, G., Learmonth, G., & Harvey, M. (2013b). Spatial attention: differential shifts in pseudoneglect direction with time-on-task and initial bias support the idea of observer subtypes. Neuropsychologia, 51(13), 2747-2756 recently presented evidence that the direction and magnitude of bias exhibited by the participant early in the task (left biased, no bias, or right biased) were stable traits that predicted the direction of the subsequent time-on-task shift in spatial bias. That is, the spatial bias of participants who were initially left biased shifted in a rightward direction with time, whereas that of participants who were initially right biased shifted in a leftward direction. If valid, the data of Benwell et al. are potentially important and may demand a re-evaluation of current models of the neural networks governing spatial attention. Here we use two novel spatial attention tasks in an attempt to confirm the results of Benwell et al. We show that rather than being indicative of true participant subtypes, these data patterns are likely driven, at least in part, by 'regression towards the mean' arising from the analysis method employed. Although evidence supports the contention that trait-like individual differences in spatial bias exist within the healthy population, no clear evidence is yet available for participant/observer subtypes in the direction of time-on-task shift in spatial biases.


Subject(s)
Attention/physiology , Brain/physiology , Space Perception/physiology , Visual Perception/physiology , Adolescent , Adult , Electroencephalography , Evoked Potentials/physiology , Female , Humans , Male , Middle Aged , Neuropsychological Tests , Young Adult
13.
Neuropsychologia ; 56: 178-83, 2014 Apr.
Article in English | MEDLINE | ID: mdl-24486422

ABSTRACT

Atypical asymmetries of spatial attention have been reported in children with attention deficit hyperactivity disorder (ADHD) and may be exacerbated by non-spatial factors such as attentional capacity. Although preliminary evidence suggests that asymmetries of attention in ADHD may be modifiable by the psychostimulant, methylphenidate, further placebo-controlled studies are required. This study first aimed to confirm recent evidence that increasing non-spatial processing load at fixation can unmask a spatial gradient of target detection in children with ADHD but not Controls. Second, we used placebo-controlled randomised trial methodology to ask whether 20mg of methylphenidate (MPH) could remediate any load-dependent asymmetry of spatial attention in adolescents with ADHD. Twelve male adolescents with ADHD were assessed twice in a double-blind, randomized design, under either placebo or an acute dose of methylphenidate. Thirteen typically developing adolescent Controls completed a single session under placebo. Participants completed a computer-based task in which they monitored a centrally presented rapid serial visual presentation stream for a probe stimulus, while also responding to brief peripheral events. The attentional load of the central task was manipulated by varying the target instructions but not the physical stimuli or the frequency of targets. Between-group analyses under placebo conditions indicated that increased attentional load induced a spatial gradient for target detection in the ADHD but not Controls, such that load slowed response times for left, but not, right hemi-field targets. This load-dependent spatial asymmetry in the adolescents with ADHD was abolished by administration of methylphenidate. Methylphenidate may "normalise" target detection between the hemi-fields in ADHD via enhancement of the right-lateralised ventral attention networks that support non-spatial attention.


Subject(s)
Attention Deficit Disorder with Hyperactivity/drug therapy , Central Nervous System Stimulants/therapeutic use , Functional Laterality/drug effects , Methylphenidate/therapeutic use , Space Perception/drug effects , Adolescent , Analysis of Variance , Child , Dose-Response Relationship, Drug , Double-Blind Method , Humans , Male , Neuropsychological Tests , Reaction Time/drug effects
14.
Neuropsychologia ; 51(7): 1215-23, 2013 Jun.
Article in English | MEDLINE | ID: mdl-23583973

ABSTRACT

Biases of spatial attention may be moderated by non-spatial factors such as attentional load and time-on-task. Although these effects are thought to arise from depletion of right hemisphere processing resources, their neurophysiological bases have yet to be confirmed. We recorded posterior α-band EEG--a marker of cortical excitability linked to spatial attention orienting--from 66 non-clinical participants who detected transient, unilateral visual targets while also monitoring stimuli at fixation. Asymmetry indices were derived for both lateral target reaction times and hemispheric differences in α-activity before and after lateral target onsets. Pre-target α became more prominent over the right, relative to left, hemisphere as the task progressed over 48-min, and this change was correlated with a significant rightward shift in spatial bias. Contrary to past studies of posterior α-asymmetry and orienting, here participants did not receive pre-target cues. Thus we show that asymmetries in the hemispheric distribution of anticipatory α are not only apparent during externally-cued attention orienting, but are also sensitive to decreasing alertness over time. These data are the first to link rightward attention drift over time with change in hemispheric activation asymmetry, providing important implications for our understanding of interacting spatial attention and non-spatial alertness networks.


Subject(s)
Attention/physiology , Bias , Brain Mapping , Brain/physiology , Functional Laterality/physiology , Space Perception/physiology , Analysis of Variance , Electroencephalography , Evoked Potentials, Visual/physiology , Female , Humans , Male , Photic Stimulation , Statistics as Topic
15.
Neuropsychologia ; 51(6): 1085-93, 2013 May.
Article in English | MEDLINE | ID: mdl-23391561

ABSTRACT

Converging evidence suggests that right-hemisphere dominant spatial attention systems can be modulated by non-spatial processes such as attentional capacity. The severity of neglect in right-hemisphere stroke patients for example, is correlated with impairments in non-lateralized attention. Evidence also suggests the coexistence of lateralized inattention and reduced capacity in developmental disorders of attention, such as attention deficit hyperactivity disorder (ADHD), which is marked by cognitive impairments suggestive of right hemisphere dysfunction. These lines of evidence argue against a coincident damage hypothesis and suggest instead a direct modulation of spatial attention by non-spatial processes. Here we sought experimental evidence for this relationship in both acquired and developmental disorders of attention. Six adult stroke patients with focal right brain injury and 19 children with ADHD were studied in comparison to control groups of both healthy older adults and typically developing children. The participants were required to detect transient, unilateral visual targets while simultaneously monitoring a stream of alphanumeric characters at fixation. Load at fixation was manipulated by asking participants either to ignore the central stream and focus on the peripheral detection task (no report condition), or to monitor the central stream for a probe item that was defined by either a unique feature (low load condition) or a conjunction of features (high load condition). As expected, in all participants greater load at fixation slowed responses to peripheral targets. Crucially, in right brain injured patients but not older healthy adults left target detection was slowed significantly more than central and right target detection. A qualitatively similar pattern was seen in children with ADHD, but not in typically developing children. The imposition of load at fixation slowed responses to left compared with right targets, and this response time asymmetry was correlated with the severity of ADHD symptoms. These results suggest that a direct manipulation of non-spatial attention can reveal lateralised attention deficits in both acquired and developmental forms of inattention. Our findings support the view that spatial attention networks are tightly integrated with non-lateralized aspects of attention.


Subject(s)
Attention Deficit Disorder with Hyperactivity/etiology , Developmental Disabilities/complications , Perceptual Disorders/chemically induced , Perceptual Disorders/etiology , Space Perception/physiology , Adolescent , Analysis of Variance , Child , Female , Functional Laterality , Humans , Magnetic Resonance Imaging , Male , Neuropsychological Tests , Photic Stimulation
16.
Neuropsychologia ; 50(12): 2823-2829, 2012 Oct.
Article in English | MEDLINE | ID: mdl-22940645

ABSTRACT

A number of recent studies suggest that DNA variation in the dopamine transporter gene (DAT1) influences spatial attention asymmetry in clinical populations such as ADHD, but confirmation in non-clinical samples is required. Since non-spatial factors such as attentional load have been shown to influence spatial biases in clinical conditions, here we sought to determine whether any association between DAT1 genotype and spatial bias might be moderated by non-spatial attentional load. Healthy adults were asked to react to sudden onset peripheral targets while demand on non-spatial attention was manipulated via a central task. Participants were genotyped for a DAT1 variable number of tandem repeat (VNTR) polymorphism. The 10-repeat allele of this variant is a replicated susceptibility allele for ADHD and has been shown to associate with spatial bias. As expected, an overall leftward asymmetry/pseudoneglect was observed when the data were averaged across the entire sample. When data were stratified by DAT1 genotype, individuals lacking homozygosity for the 10-repeat DAT1 allele (non-10/10) showed a pronounced leftward bias that was significantly different from zero. In line with past reports from children with ADHD, this leftward bias was attenuated in individuals who were homozygous for the DAT1 10-repeat allele (10/10), suggestive of relatively weaker right hemisphere dominance for spatial attention. This effect of DAT1 genotype on spatial bias was not modulated by non-spatial attention load. These data confirm in healthy adult participants both the existence and the direction of the relationship previously reported between DAT1 genotype and spatial bias in children with ADHD. These data add to a growing body of evidence showing that spatial attentional asymmetry is a stable quantitative trait, with individual differences in this trait significantly predicted by common DNA variation in the DAT1 gene.


Subject(s)
Attention/physiology , Dopamine Plasma Membrane Transport Proteins/genetics , Dopamine/physiology , Individuality , Adolescent , Adult , Alleles , Female , Genetic Predisposition to Disease , Genotype , Homozygote , Humans , Male , Middle Aged , Minisatellite Repeats , Perceptual Disorders/genetics , Phenotype , Polymorphism, Genetic
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