Evidence Accumulation Rate Moderates the Relationship between Enriched Environment Exposure and Age-Related Response Speed Declines.

Older adults exposed to enriched environments (EEs) maintain relatively higher levels of cognitive function, even in the face of compromised markers of brain health. Response speed (RS) is often used as a simple proxy to measure the preservation of global cognitive function in older adults. However, it is unknown which specific selection, decision, and/or motor processes provide the most specific indices of neurocognitive health. Here, using a simple decision task with electroencephalography (EEG), we found that the efficiency with which an individual accumulates sensory evidence was a critical determinant of the extent to which RS was preserved in older adults (63% female, 37% male). Moreover, the mitigating influence of EE on age-related RS declines was most pronounced when evidence accumulation rates were shallowest. These results suggest that the phenomenon of cognitive reserve, whereby high EE individuals can better tolerate suboptimal brain health to facilitate the preservation of cognitive function, is not just applicable to neuroanatomical indicators of brain aging but can be observed in markers of neurophysiology. Our results suggest that EEG metrics of evidence accumulation may index neurocognitive vulnerability of the aging brain.Significance Statement Response speed in older adults is closely linked with trajectories of cognitive aging. Here, by recording brain activity while individuals perform a simple computer task, we identify a neural metric that is a critical determinant of response speed. Older adults exposed to greater cognitive and social stimulation throughout a lifetime could maintain faster responding, even when this neural metric was impaired. This work suggests EEG is a useful technique for interrogating how a lifetime of stimulation benefits brain health in aging.

Evidence accumulation during perceptual decisions in humans varies as a function of dorsal frontoparietal organization.

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.

The role of premature evidence accumulation in making difficult perceptual decisions under temporal uncertainty.

The computations and neural processes underpinning decision making have primarily been investigated using highly simplified tasks in which stimulus onsets cue observers to start accumulating choice-relevant information. Yet, in daily life we are rarely afforded the luxury of knowing precisely when choice-relevant information will appear. Here, we examined neural indices of decision formation while subjects discriminated subtle stimulus feature changes whose timing relative to stimulus onset ('foreperiod') was uncertain. Joint analysis of behavioural error patterns and neural decision signal dynamics indicated that subjects systematically began the accumulation process before any informative evidence was presented, and further, that accumulation onset timing varied systematically as a function of the foreperiod of the preceding trial. These results suggest that the brain can adjust to temporal uncertainty by strategically modulating accumulation onset timing according to statistical regularities in the temporal structure of the sensory environment with particular emphasis on recent experience.

Behavioural and neural signatures of perceptual decision-making are modulated by pupil-linked arousal.

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.

Catecholamine Modulation of Evidence Accumulation during Perceptual Decision Formation: A Randomized Trial.

Recent behavioral modeling and pupillometry studies suggest that neuromodulatory arousal systems play a role in regulating decision formation but neurophysiological support for these observations is lacking. We employed a randomized, double-blinded, placebo-controlled, crossover design to probe the impact of pharmacological enhancement of catecholamine levels on perceptual decision-making. Catecholamine levels were manipulated using the clinically relevant drugs methylphenidate and atomoxetine, and their effects were compared with those of citalopram and placebo. Participants performed a classic EEG oddball paradigm that elicits the P3b, a centro-parietal potential that has been shown to trace evidence accumulation, under each of the four drug conditions. We found that methylphenidate and atomoxetine administration shortened RTs to the oddball targets. The neural basis of this behavioral effect was an earlier P3b peak latency, driven specifically by an increase in its buildup rate without any change in its time of onset or peak amplitude. This study provides neurophysiological evidence for the catecholaminergic enhancement of a discrete aspect of human decision-making, that is, evidence accumulation. Our results also support theoretical accounts suggesting that catecholamines may enhance cognition via increases in neural gain.

Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation.

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.

A gaze independent hybrid-BCI based on visual spatial attention.

OBJECTIVE: Brain-computer interfaces (BCI) use measures of brain activity to convey a user's intent without the need for muscle movement. Hybrid designs, which use multiple measures of brain activity, have been shown to increase the accuracy of BCIs, including those based on EEG signals reflecting covert attention. Our study examined whether incorporating a measure of the P3 response improved the performance of a previously reported attention-based BCI design that incorporates measures of steady-state visual evoked potentials (SSVEP) and alpha band modulations. APPROACH: Subjects viewed stimuli consisting of two bi-laterally located flashing white boxes on a black background. Streams of letters were presented sequentially within the boxes, in random order. Subjects were cued to attend to one of the boxes without moving their eyes, and they were tasked with counting the number of target-letters that appeared within. P3 components evoked by target appearance, SSVEPs evoked by the flashing boxes, and power in the alpha band are modulated by covert attention, and the modulations can be used to classify trials as left-attended or right-attended. MAIN RESULTS: We showed that classification accuracy was improved by including a P3 feature along with the SSVEP and alpha features (the inclusion of a P3 feature lead to a 9% increase in accuracy compared to the use of SSVEP and Alpha features alone). We also showed that the design improves the robustness of BCI performance to individual subject differences. SIGNIFICANCE: These results demonstrate that incorporating multiple neurophysiological indices of covert attention can improve performance in a gaze-independent BCI.

Visuospatial Asymmetries Arise from Differences in the Onset Time of Perceptual Evidence Accumulation.

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.

Ocular exposure to blue-enriched light has an asymmetric influence on neural activity and spatial attention.

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.

Target Selection Signals Influence Perceptual Decisions by Modulating the Onset and Rate of Evidence Accumulation.

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.

Behavioral and electrophysiological evidence of opposing lateral visuospatial asymmetries in the upper and lower visual fields.

Neurologically healthy individuals typically exhibit a subtle bias towards the left visual field during spatial judgments, known as "pseudoneglect". However, it has yet to be reliably established if the direction and magnitude of this lateral bias varies along the vertical plane. Here, participants were required to distribute their attention equally across a checkerboard array spanning the entire visual field in order to detect transient targets that appeared at unpredictable locations. Reaction times (RTs) were faster to left hemifield targets in the lower visual field but the opposite trend was observed for targets in the upper field. Electroencephalogram (EEG) analyses focused on the interval prior to target onset in order to identify endogenous neural correlates of these behavioral asymmetries. The relative hemispheric distribution of pre-target oscillatory alpha power was predictive of RT bias to targets in the lower visual field but not the upper field, indicating separate attentional mechanisms for the upper and lower visual fields. Analysis of multifocal visual-evoked potentials (MVEP) in the pre-target interval also indicated that the opposing upper and lower field asymmetries may impact on the magnitude of primary visual cortical responses. These results provide new evidence of a functional segregation of upper and lower field visuospatial processing.

Differential shift in spatial bias over time depends on observers׳ initial bias: Observer subtypes, or regression to the mean?

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.

Endogenous auditory frequency-based attention modulates electroencephalogram-based measures of obligatory sensory activity in humans.

Auditory selective attention is the ability to enhance the processing of a single sound source, while simultaneously suppressing the processing of other competing sound sources. Recent research has addressed a long-running debate by showing that endogenous attention produces effects on obligatory sensory responses to continuous and competing auditory stimuli. However, until now, this result has only been shown under conditions where the competing stimuli differed in both their frequency characteristics and, importantly, their spatial location. Thus, it is unknown whether endogenous selective attention based only on nonspatial features modulates obligatory sensory processing. Here, we investigate this issue using a diotic paradigm, such that competing auditory stimuli differ in frequency, but had no separation in space. We find a significant effect of attention on electroencephalogram-based measures of obligatory sensory processing at several poststimulus latencies. We discuss these results in terms of previous research on feature-based attention and by comparing our findings with the previous work using stimuli that differed both in terms of spatial and frequency-based characteristics.

Towards a gaze-independent hybrid-BCI based on SSVEPs, alpha-band modulations and the P300.

In recent years it has been shown to be possible to create a Brain Computer Interface (BCI) using non-invasive electroencephalographic (EEG) measurements of covert visual spatial attention. For example, that both Steady-State Visual Evoked Potentials (SSVEP) and parieto-occipital alpha band activity have been shown to be sensitive to covert attention and this has been exploited to provide simple communication control without the need for any physical movement. In this study, potential improvements in the speed and accuracy of such a BCI are investigated by exploring the possibility of incorporating a P300 task into an SSVEP covert attention paradigm. Should this be possible it would pave the way for a gaze-independent hybrid BCI based on three somewhat independent EEG signals. Within a well-established SSVEP-based attention paradigm we show that it is possible to make a binary classification of covert attention using just the P300 with an average accuracy of 71% across three subjects. We also validate previously published research by showing robust attention effects on the SSVEP and alpha band activity within this paradigm. In future work, it is hoped that by integrating the three signals into a hybrid BCI a significant improvement in performance will be forthcoming leading to an easily usable real time communication device for patients with severe disabilities such as Locked-In Syndrome (LIS).