Arterial oxygen desaturation during moderate hypoxia hinders sensorimotor performance.

INTRODUCTION: Moderate hypoxia may impact cognitive and sensorimotor performance prior to self-recognized impairments. Therefore, rapid and objective assessment tools to identify people at risk of impaired function during moderate hypoxia is needed. PURPOSE: Test the hypothesis that reductions in arterial oxygen saturation during moderate normobaric hypoxia (FiO2 = 14%) decreases gamified sensorimotor performance as measured by alterations of motor acuity. METHODS: Following three consecutive days of practice, thirty healthy adults (25 ± 5 y, 10 females) completed three bouts of the tablet-based gamified assessment (Statespace Labs, Inc.) of motor acuity at Baseline and 60 and 90 min after exposure to 13.8 ± 0.2% (hypoxia) and 20.1 ± 0.4% (normoxia) oxygen. The gamified assessment involved moving the tablet to aim and shoot at targets. Both conditions were completed on the same day and were administered in a single-blind, block randomized manner. Performance metrics included shot time and shot variability. Arterial oxyhemoglobin saturation estimated via forehead pulse oximetry (SpO2). Data were analyzed using linear mixed effects models. RESULTS: Compared to normoxia (99±1%), SpO2 was lower (p<0.001) at 60 (89±3%) and 90 (90±2%) min of hypoxia. Shot time was unaffected by decreases in SpO2 (0.012, p = 0.19). Nor was shot time affected by the interaction between SpO2 decrease and baseline performance (0.006, p = 0.46). Shot variability was greater (i.e., less precision, worse performance) with decreases in SpO2 (0.023, p = 0.02) and depended on the interaction between SpO2 decrease and baseline performance (0.029, p< 0.01). CONCLUSION: Decreases in SpO2 during moderate hypoxic exposure hinders sensorimotor performance via decreased motor acuity, i.e., greater variability (less precision) with no change in speed with differing decreases in SpO2. Thus, personnel who are exposed to moderate hypoxia and have greater decreases in SpO2 exhibit lower motor acuity, i.e., less precise movements even though decision time and movement speed are unaffected.

Gamified assessment of cognitive performance during moderate hypoxia.

INTRODUCTION: There is a need for rapid and objective assessment tools to identify people at risk of impaired cognitive function during hypoxia. PURPOSE: To test the hypotheses that performance on gamified cognitive tests examining the cognitive domains of executive function (Gridshot), working memory (Capacity) and spatial tracking (Multitracker) will be reduced during normobaric exposure to moderate normobaric hypoxia. METHODS: Following three consecutive days of practice, twenty-one healthy adults (27 ± 5 y, 9 females) completed five 1-min rounds of the tablet-based games Gridshot, Capacity, and Multitracker (Statespace Labs, Inc.) at Baseline and 60 and 90 min after exposure to 14.0 ± 0.2% (hypoxia) and 20.6 ± 0.3% (normoxia) oxygen. Both conditions were completed on the same day and were administered in a single-blind, block randomized manner. Arterial oxyhemoglobin saturation was estimated via forehead pulse oximetry (SpO2). Data were analyzed using ANCOVA with a covariate of Baseline. RESULTS: Compared to normoxia (98 ± 1%), SpO2 was lower (p < 0.001) at 60 (91 ± 3%) and 90 (91 ± 2%) min of hypoxia. No condition x time interaction effects were identified for any gamified cognitive tests (p ≥ 0.32). A main effect of condition was identified for Capacity (p = 0.05) and Multitracker (p = 0.04), but not Gridshot (p = 0.33). Post hoc analyses of the composite scores for both Capacity (p = 0.11) and Multitracker (p = 0.73) demonstrated no difference between conditions. CONCLUSION: Performance on gamified cognitive tests was not consistently affected by acute normobaric moderate hypoxic exposure.

The visible gorilla: Unexpected fast-not physically salient-Objects are noticeable.

It is widely believed that observers can fail to notice clearly visible unattended objects, even if they are moving. Here, we created parametric tasks to test this belief and report the results of three high-powered experiments (total n = 4,493) indicating that this effect is strongly modulated by the speed of the unattended object. Specifically, fast-but not slow-objects are readily noticeable, whether they are attended or not. These results suggest that fast motion serves as a potent exogenous cue that overrides task-focused attention, showing that fast speeds, not long exposure duration or physical salience, strongly diminish inattentional blindness effects.

Assessment of human expertise and movement kinematics in first-person shooter games.

In contrast to traditional professional sports, there are few standardized metrics in professional esports (competitive multiplayer video games) for assessing a player's skill and ability. We assessed the performance of professional-level players in Aim LabTM, a first-person shooter training and assessment game, with two target-shooting tasks. These tasks differed primarily in target size: the task with large targets provided an incentive to be fast but imprecise and the task with large targets provided an incentive to be precise but slow. Each player's motor acuity was measured by characterizing the speed-accuracy trade-off in shot behavior: shot time (elapsed time for a player to shoot at a target) and shot spatial error (distance from center of a target). We also characterized the fine-grained kinematics of players' mouse movements. Our findings demonstrate that: 1) movement kinematics depended on task demands; 2) individual differences in motor acuity were significantly correlated with kinematics; and 3) performance, combined across the two target sizes, was poorly characterized by Fitts Law. Our approach to measuring motor acuity has widespread applications not only in esports assessment and training, but also in basic (motor psychophysics) and clinical (gamified rehabilitation) research.

Task-related hemodynamic responses in human early visual cortex are modulated by task difficulty and behavioral performance.

Early visual cortex exhibits widespread hemodynamic responses in the absence of visual stimulation, which are entrained to the timing of a task and not predicted by local spiking or local field potential. Such task-related responses (TRRs) covary with reward magnitude and physiological signatures of arousal. It is unknown, however, if TRRs change on a trial-to-trial basis according to behavioral performance and task difficulty. If so, this would suggest that TRRs reflect arousal on a trial-to-trial timescale and covary with critical task and behavioral variables. We measured functional magnetic resonance imaging blood-oxygen-level-dependent (fMRI-BOLD) responses in the early visual cortex of human observers performing an orientation discrimination task consisting of separate easy and hard runs of trials. Stimuli were presented in a small portion of one hemifield, but the fMRI response was measured in the ipsilateral hemisphere, far from the stimulus representation and focus of spatial attention. TRRs scaled in amplitude with task difficulty, behavioral accuracy, reaction time, and lapses across trials. These modulations were not explained by the influence of respiration, cardiac activity, or head movement on the fMRI signal. Similar modulations with task difficulty and behavior were observed in pupil size. These results suggest that TRRs reflect arousal and behavior on the timescale of individual trials.

A unified model of the task-evoked pupil response.

The pupil dilates and reconstricts following task events. It is popular to model this task-evoked pupil response as a linear transformation of event-locked impulses, whose amplitudes are used as estimates of arousal. We show that this model is incorrect and propose an alternative model based on the physiological finding that a common neural input drives saccades and pupil size. The estimates of arousal from our model agreed with key predictions: Arousal scaled with task difficulty and behavioral performance but was invariant to small differences in trial duration. Moreover, the model offers a unified explanation for a wide range of phenomena: entrainment of pupil size and saccades to task timing, modulation of pupil response amplitude and noise with task difficulty, reaction time-dependent modulation of pupil response timing and amplitude, a constrictory pupil response time-locked to saccades, and task-dependent distortion of this saccade-locked pupil response.

Spared perilesional V1 activity underlies training-induced recovery of luminance detection sensitivity in cortically-blind patients.

Damage to the primary visual cortex (V1) causes homonymous visual-field loss long considered intractable. Multiple studies now show that perceptual training can restore visual functions in chronic cortically-induced blindness (CB). A popular hypothesis is that training can harness residual visual functions by recruiting intact extrageniculostriate pathways. Training may also induce plastic changes within spared regions of the damaged V1. Here, we link changes in luminance detection sensitivity with retinotopic fMRI activity before and after visual discrimination training in eleven patients with chronic, stroke-induced CB. We show that spared V1 activity representing perimetrically-blind locations prior to training predicts the amount of training-induced recovery of luminance detection sensitivity. Additionally, training results in an enlargement of population receptive fields in perilesional V1, which increases blind-field coverage and may support further recovery with subsequent training. These findings uncover fundamental changes in perilesional V1 cortex underlying training-induced restoration of conscious luminance detection sensitivity in CB.

An image-computable model of how endogenous and exogenous attention differentially alter visual perception.

Attention alters perception across the visual field. Typically, endogenous (voluntary) and exogenous (involuntary) attention similarly improve performance in many visual tasks, but they have differential effects in some tasks. Extant models of visual attention assume that the effects of these two types of attention are identical and consequently do not explain differences between them. Here, we develop a model of spatial resolution and attention that distinguishes between endogenous and exogenous attention. We focus on texture-based segmentation as a model system because it has revealed a clear dissociation between both attention types. For a texture for which performance peaks at parafoveal locations, endogenous attention improves performance across eccentricity, whereas exogenous attention improves performance where the resolution is low (peripheral locations) but impairs it where the resolution is high (foveal locations) for the scale of the texture. Our model emulates sensory encoding to segment figures from their background and predict behavioral performance. To explain attentional effects, endogenous and exogenous attention require separate operating regimes across visual detail (spatial frequency). Our model reproduces behavioral performance across several experiments and simultaneously resolves three unexplained phenomena: 1) the parafoveal advantage in segmentation, 2) the uniform improvements across eccentricity by endogenous attention, and 3) the peripheral improvements and foveal impairments by exogenous attention. Overall, we unveil a computational dissociation between each attention type and provide a generalizable framework for predicting their effects on perception across the visual field.

A dynamic normalization model of temporal attention.

Vision is dynamic, handling a continuously changing stream of input, yet most models of visual attention are static. Here, we develop a dynamic normalization model of visual temporal attention and constrain it with new psychophysical human data. We manipulated temporal attention-the prioritization of visual information at specific points in time-to a sequence of two stimuli separated by a variable time interval. Voluntary temporal attention improved perceptual sensitivity only over a specific interval range. To explain these data, we modelled voluntary and involuntary attentional gain dynamics. Voluntary gain enhancement took the form of a limited resource over short time intervals, which recovered over time. Taken together, our theoretical and experimental results formalize and generalize the idea of limited attentional resources across space at a single moment to limited resources across time at a single location.

Long-Term Motor Learning in the "Wild" With High Volume Video Game Data.

Motor learning occurs over long periods of practice during which motor acuity, the ability to execute actions more accurately, precisely, and in less time, improves. Laboratory-based studies of motor learning are typically limited to a small number of participants and a time frame of minutes to several hours per participant. There is a need to assess the generalizability of theories and findings from lab-based motor learning studies on larger samples and time scales. In addition, laboratory-based studies of motor learning use relatively simple motor tasks which participants are unlikely to be intrinsically motivated to learn, limiting the interpretation of their findings in more ecologically valid settings ("in the wild"). We studied the acquisition and longitudinal refinement of a complex sensorimotor skill embodied in a first-person shooter video game scenario, with a large sample size (N = 7174, 682,564 repeats of the 60 s game) over a period of months. Participants voluntarily practiced the gaming scenario for up to several hours per day up to 100 days. We found improvement in performance accuracy (quantified as hit rate) was modest over time but motor acuity (quantified as hits per second) improved considerably, with 40-60% retention from 1 day to the next. We observed steady improvements in motor acuity across multiple days of video game practice, unlike most motor learning tasks studied in the lab that hit a performance ceiling rather quickly. Learning rate was a non-linear function of baseline performance level, amount of daily practice, and to a lesser extent, number of days between practice sessions. In addition, we found that the benefit of additional practice on any given day was non-monotonic; the greatest improvements in motor acuity were evident with about an hour of practice and 90% of the learning benefit was achieved by practicing 30 min per day. Taken together, these results provide a proof-of-concept in studying motor skill acquisition outside the confines of the traditional laboratory, in the presence of unmeasured confounds, and provide new insights into how a complex motor skill is acquired in an ecologically valid setting and refined across much longer time scales than typically explored.

Heading perception depends on time-varying evolution of optic flow.

There is considerable support for the hypothesis that perception of heading in the presence of rotation is mediated by instantaneous optic flow. This hypothesis, however, has never been tested. We introduce a method, termed "nonvarying phase motion," for generating a stimulus that conveys a single instantaneous optic flow field, even though the stimulus is presented for an extended period of time. In this experiment, observers viewed stimulus videos and performed a forced-choice heading discrimination task. For nonvarying phase motion, observers made large errors in heading judgments. This suggests that instantaneous optic flow is insufficient for heading perception in the presence of rotation. These errors were mostly eliminated when the velocity of phase motion was varied over time to convey the evolving sequence of optic flow fields corresponding to a particular heading. This demonstrates that heading perception in the presence of rotation relies on the time-varying evolution of optic flow. We hypothesize that the visual system accurately computes heading, despite rotation, based on optic acceleration, the temporal derivative of optic flow.

Differential impact of endogenous and exogenous attention on activity in human visual cortex.

How do endogenous (voluntary) and exogenous (involuntary) attention modulate activity in visual cortex? Using ROI-based fMRI analysis, we measured fMRI activity for valid and invalid trials (target at cued/un-cued location, respectively), pre- or post-cueing endogenous or exogenous attention, while participants performed the same orientation discrimination task. We found stronger modulation in contralateral than ipsilateral visual regions, and higher activity in valid- than invalid-trials. For endogenous attention, modulation of stimulus-evoked activity due to a pre-cue increased along the visual hierarchy, but was constant due to a post-cue. For exogenous attention, modulation of stimulus-evoked activity due to a pre-cue was constant along the visual hierarchy, but was not modulated due to a post-cue. These findings reveal that endogenous and exogenous attention distinctly modulate activity in visuo-occipital areas during orienting and reorienting; endogenous attention facilitates both the encoding and the readout of visual information whereas exogenous attention only facilitates the encoding of information.

A recurrent circuit implements normalization, simulating the dynamics of V1 activity.

The normalization model has been applied to explain neural activity in diverse neural systems including primary visual cortex (V1). The model's defining characteristic is that the response of each neuron is divided by a factor that includes a weighted sum of activity of a pool of neurons. Despite the success of the normalization model, there are three unresolved issues. 1) Experimental evidence supports the hypothesis that normalization in V1 operates via recurrent amplification, i.e., amplifying weak inputs more than strong inputs. It is unknown how normalization arises from recurrent amplification. 2) Experiments have demonstrated that normalization is weighted such that each weight specifies how one neuron contributes to another's normalization pool. It is unknown how weighted normalization arises from a recurrent circuit. 3) Neural activity in V1 exhibits complex dynamics, including gamma oscillations, linked to normalization. It is unknown how these dynamics emerge from normalization. Here, a family of recurrent circuit models is reported, each of which comprises coupled neural integrators to implement normalization via recurrent amplification with arbitrary normalization weights, some of which can recapitulate key experimental observations of the dynamics of neural activity in V1.

Uncharacteristic Task-Evoked Pupillary Responses Implicate Atypical Locus Ceruleus Activity in Autism.

Autism spectrum disorder (ASD) is characterized partly by atypical attentional engagement, reflected in exaggerated and variable responses to sensory stimuli. Attentional engagement is known to be regulated by the locus ceruleus (LC). Moderate baseline LC activity globally dampens neural responsivity and is associated with adaptive deployment and narrowing of attention to task-relevant stimuli. In contrast, increased baseline LC activity enhances neural responsivity across cortex and widening of attention to environmental stimuli regardless of their task relevance. Given attentional atypicalities in ASD, this study is the first to evaluate whether, under different attentional task demands, individuals with ASD exhibit a different profile of LC activity compared with typically developing controls. Males and females with ASD and age- and gender-matched controls participated in a one-back letter detection test while task-evoked pupillary responses, an established correlate for LC activity, were recorded. Participants completed this task in two conditions, either in the absence or presence of distractor auditory tones. Compared with controls, individuals with ASD evinced atypical pupillary responses in the presence versus absence of distractors. Notably, this atypical pupillary profile was evident despite the fact that both groups exhibited equivalent task performance. Moreover, between-group differences in pupillary responses were observed specifically in response to task-relevant events, providing confirmation that the group differences most likely were specifically associated with distinctions in LC activity. These findings suggest that individuals with ASD show atypical modulation of LC activity with changes in attentional demands, offering a possible mechanistic and neurobiological account for attentional atypicalities in ASD.SIGNIFICANCE STATEMENT Individuals with autism spectrum disorder (ASD) exhibit atypical attentional behaviors, including altered sensory responses and atypical fixedness, but the neural mechanism underlying these behaviors remains elusive. One candidate mechanism is atypical locus ceruleus (LC) activity, as the LC plays a critical role in attentional modulation. Specifically, LC activity is involved in regulating the trade-off between environmental exploration and focused attention. This study shows that, under tightly controlled conditions, task-evoked pupil responses, an LC activity proxy, are lower in individuals with ASD than in controls, but only in the presence of task-irrelevant stimuli. This suggests that individuals with ASD evince atypical modulation of LC activity in accordance with changes in attentional demands, offering a mechanistic account for attentional atypicalities in ASD.

Contingent adaptation in masking and surround suppression.

Adaptation is the process that changes a neuron's response based on recent inputs. In the traditional model, a neuron's state of adaptation depends on the recent input to that neuron alone, whereas in a recently introduced model (Hebbian normalization), adaptation depends on the structure of neural correlated firing. In particular, increased response products between pairs of neurons leads to increased mutual suppression. We test a psychophysical prediction of this model: adaptation should depend on 2nd-order statistics of input stimuli. That is, if two stimuli excite two distinct sub-populations of neurons, then presenting those stimuli simultaneously during adaptation should strengthen mutual suppression between those subpopulations. We confirm this prediction in two experiments. In the first, pairing two gratings synchronously during adaptation (i.e., a plaid) rather than asynchronously (interleaving the two gratings in time) leads to increased effectiveness of one pattern for masking the other. In the second, pairing the gratings in a center-surround configuration results in reduced apparent contrast for the central grating when paired with the same surround (as compared with a condition in which the central grating appears with a different surround at test than during adaptation). These results are consistent with the prediction that an increase in response covariance leads to greater mutual suppression between neurons. This effect is detectable both at threshold (masking) and well above threshold (apparent contrast).

Position-theta-phase model of hippocampal place cell activity applied to quantification of running speed modulation of firing rate.

Spiking activity of place cells in the hippocampus encodes the animal's position as it moves through an environment. Within a cell's place field, both the firing rate and the phase of spiking in the local theta oscillation contain spatial information. We propose a position-theta-phase (PTP) model that captures the simultaneous expression of the firing-rate code and theta-phase code in place cell spiking. This model parametrically characterizes place fields to compare across cells, time, and conditions; generates realistic place cell simulation data; and conceptualizes a framework for principled hypothesis testing to identify additional features of place cell activity. We use the PTP model to assess the effect of running speed in place cell data recorded from rats running on linear tracks. For the majority of place fields, we do not find evidence for speed modulation of the firing rate. For a small subset of place fields, we find firing rates significantly increase or decrease with speed. We use the PTP model to compare candidate mechanisms of speed modulation in significantly modulated fields and determine that speed acts as a gain control on the magnitude of firing rate. Our model provides a tool that connects rigorous analysis with a computational framework for understanding place cell activity.

Oscillatory recurrent gated neural integrator circuits (ORGaNICs), a unifying theoretical framework for neural dynamics.

Working memory is an example of a cognitive and neural process that is not static but evolves dynamically with changing sensory inputs; another example is motor preparation and execution. We introduce a theoretical framework for neural dynamics, based on oscillatory recurrent gated neural integrator circuits (ORGaNICs), and apply it to simulate key phenomena of working memory and motor control. The model circuits simulate neural activity with complex dynamics, including sequential activity and traveling waves of activity, that manipulate (as well as maintain) information during working memory. The same circuits convert spatial patterns of premotor activity to temporal profiles of motor control activity and manipulate (e.g., time warp) the dynamics. Derivative-like recurrent connectivity, in particular, serves to manipulate and update internal models, an essential feature of working memory and motor execution. In addition, these circuits incorporate recurrent normalization, to ensure stability over time and robustness with respect to perturbations of synaptic weights.

Corrigendum: Analysis of Perceptual Expertise in Radiology - Current Knowledge and a New Perspective.

[This corrects the article DOI: 10.3389/fnhum.2019.00213.].

Analysis of Perceptual Expertise in Radiology - Current Knowledge and a New Perspective.

Radiologists rely principally on visual inspection to detect, describe, and classify findings in medical images. As most interpretive errors in radiology are perceptual in nature, understanding the path to radiologic expertise during image analysis is essential to educate future generations of radiologists. We review the perceptual tasks and challenges in radiologic diagnosis, discuss models of radiologic image perception, consider the application of perceptual learning methods in medical training, and suggest a new approach to understanding perceptional expertise. Specific principled enhancements to educational practices in radiology promise to deepen perceptual expertise among radiologists with the goal of improving training and reducing medical error.

Temporal Contingencies Determine Whether Adaptation Strengthens or Weakens Normalization.

A fundamental and nearly ubiquitous feature of sensory encoding is that neuronal responses are strongly influenced by recent experience, or adaptation. Theoretical and computational studies have proposed that many adaptation effects may result in part from changes in the strength of normalization signals. Normalization is a "canonical" computation in which a neuron's response is modulated (normalized) by the pooled activity of other neurons. Here, we test whether adaptation can alter the strength of cross-orientation suppression, or masking, a paradigmatic form of normalization evident in primary visual cortex (V1). We made extracellular recordings of V1 neurons in anesthetized male macaques and measured responses to plaid stimuli composed of two overlapping, orthogonal gratings before and after prolonged exposure to two distinct adapters. The first adapter was a plaid consisting of orthogonal gratings and led to stronger masking. The second adapter presented the same orthogonal gratings in an interleaved manner and led to weaker masking. The strength of adaptation's effects on masking depended on the orientation of the test stimuli relative to the orientation of the adapters, but was independent of neuronal orientation preference. Changes in masking could not be explained by altered neuronal responsivity. Our results suggest that normalization signals can be strengthened or weakened by adaptation depending on the temporal contingencies of the adapting stimuli. Our findings reveal an interplay between two widespread computations in cortical circuits, adaptation and normalization, that enables flexible adjustments to the structure of the environment, including the temporal relationships among sensory stimuli.SIGNIFICANCE STATEMENT Two fundamental features of sensory responses are that they are influenced by adaptation and that they are modulated by the activity of other nearby neurons via normalization. Our findings reveal a strong interaction between these two aspects of cortical computation. Specifically, we show that cross-orientation masking, a form of normalization, can be strengthened or weakened by adaptation depending on the temporal contingencies between sensory inputs. Our findings support theoretical proposals that some adaptation effects may involve altered normalization and offer a network-based explanation for how cortex adjusts to current sensory demands.