Eye movements during motor imagery and execution reveal different visuomotor control strategies in manual interception.

Previous research has investigated the degree of congruency in gaze metrics between action execution (AE) and motor imagery (MI) for similar manual tasks. Although eye movement dynamics seem to be limited to relatively simple actions toward static objects, there is little evidence of how gaze parameters change during imagery as a function of more dynamic spatial and temporal task demands. This study examined the similarities and differences in eye movements during AE and MI for an interception task. Twenty-four students were asked to either mentally simulate or physically intercept a moving target on a computer display. Smooth pursuit, saccades, and response time were compared between the two conditions. The results show that MI was characterized by higher smooth pursuit gain and duration while no meaningful differences were found in the other parameters. The findings indicate that eye movements during imagery are not simply a duplicate of what happens during actual performance. Instead, eye movements appear to vary as a function of the interaction between visuomotor control strategies and task demands.

Eyes don't lie: Eye movements differ during covert and overt autobiographical recall.

In everyday life, autobiographical memories are revisited silently (i.e., covert recall) or shared with others (i.e., overt recall), yet most research regarding eye movements and autobiographical recall has focused on overt recall. With that in mind, the aim of the current study was to evaluate eye movements during the retrieval of autobiographical memories (with a focus on emotion), recollected during covert and overt recall. Forty-three participants recalled personal memories out loud and silently, while wearing eye-tracking glasses, and rated these memories in terms of mental imagery and emotional intensity. Analyses showed fewer and longer fixations, fewer and shorter saccades, and fewer blinks during covert recall compared with overt recall. Participants perceived more mental images and had a more intense emotional experience during covert recall. These results are discussed considering cognitive load theories and the various functions of autobiographical recall. We theorize that fewer and longer fixations during covert recall may be due to more intense mental imagery. This study enriches the field of research on eye movements and autobiographical memory by addressing how we retrieve memories silently, a common activity of everyday life. More broadly, our results contribute to building objective tools to measure autobiographical memory, alongside already existing subjective scales.

"Look at the future": Maintained fixation impoverishes future thinking.

We evaluated the relationship between eye movements and future thinking. More specifically, we evaluated whether maintained fixation could influence cognitive characteristics of future thinking. We invited participants to imagine future events in two conditions: while freely exploring a white wall and while fixating a cross on the wall. Results demonstrated fewer and longer fixations, as well as fewer and shorter saccades during maintained fixation condition than in the free gaze condition. Shorter total amplitude of saccades was also observed during the maintained fixation condition than during the free-gaze condition. Regarding the cognitive characteristics of future thinking, fewer spatiotemporal details and less visual imagery, slower retrieval time, and shorter descriptions were observed for future thinking during maintained fixation than during free-gaze condition. These results demonstrate that maintaining fixation results in an effortful construction of future scenarios. We suggest that maintained fixation limits the cognitive resources that are required for future thinking.

Corollary discharge: Linking saccades and memory circuits in the human brain.

A new study has found that, in primates with highly specialized visual systems, a corollary discharge of motor commands to make exploratory saccades arises in the midbrain, propagates to the thalamus, and then reaches hippocampal circuits in the depths of the temporal lobe where it shapes the making of memories.

Suppression head impulse test paradigm (SHIMP) characteristics in people with Parkinson's disease compared to healthy controls.

The suppression head impulse test paradigm (SHIMP) is a newly described indicator of vestibular function which yields two measures: vestibulo-ocular reflex (VOR) gain and a saccadic response. It is an alternative and complementary test to the head impulse test paradigm (HIMP). Parkinson's disease (PD) has known saccadic and central vestibular pathway dysfunction. This paper is the first description of SHIMP VOR gain and saccade characteristic in this population. This prospective observational study measured the SHIMP VOR gain and saccade characteristics in 39 participants with idiopathic PD and compared this to 40 healthy controls (HC). The effect of group, demographic variables and SHIMP characteristics were evaluated. SHIMP VOR gains were not significantly different between groups (p = 0.10). Compared to HC, the PD group mean SHIMP peak saccade velocity was significantly reduced by an average of 77.07°/sec (p < 0.001), and SHIMP saccade response latency was longer, with an average delay of 23.5 ms (p = 0.003). SHIMP saccade peak velocity was also associated with both head impulse velocity (p = 0.002) and SHIMP VOR gain (p = 0.004) variables, but there was no significant influence of these variables when SHIMP saccade peak velocity was considered as a predictor of PD (p = 0.52-0.91). VOR gains were unaffected by PD. PD-specific saccadic dysfunction, namely reduced peak saccade velocities and prolonged response latencies, were observed in the SHIMP-induced saccade responses. VOR gain using slow phase eye velocity is preferred as the indicator of vestibular function in the SHIMPs paradigm as non-vestibular factors affected saccade peak velocity.

Neuro-Ophthalmological Findings in Early Fatal Familial Insomnia.

Fatal familial insomnia (FFI) is a rare inherited prion disease characterized by sleep, autonomic, and motor disturbances. Neuro-ophthalmological abnormalities have been reported at the onset of disease, although not further characterized. We analyzed video recordings of eye movements of 6 patients with FFI from 3 unrelated kindreds, seen within 6 months from the onset of illness. Excessive saccadic intrusions were the most prominent findings. In patients with severe insomnia, striking saccadic intrusions are an early diagnostic clue for FFI. The fact that the thalamus is the first structure affected in FFI also suggests its role in the control of steady fixation. ANN NEUROL 2021;89:823-827.

Background luminance effects on pupil size associated with emotion and saccade preparation.

Pupil dilation is consistently evoked by affective and cognitive processing, and this dilation can result from sympathetic activation or parasympathetic inhibition. The relative contributions of the sympathetic and parasympathetic systems on the pupillary response induced by emotion and cognition may be different. Sympathetic and parasympathetic activity is regulated by global luminance level. Higher luminance levels lead to greater activation of the parasympathetic system while lower luminance levels lead to greater activation of the sympathetic system. To understand the contributions of the sympathetic and parasympathetic nervous systems to pupillary responses associated with emotion and saccade preparation, emotional auditory stimuli were presented following the fixation cue whose color indicated instruction to perform a pro- or anti-saccade while varying the background luminance level. Pupil dilation was evoked by emotional auditory stimuli and modulated by arousal level. More importantly, greater pupil dilation was observed with a dark background, compared to a bright background. In contrast, pupil dilation responses associated with saccade preparation were larger with the bright background than the dark background. Together, these results suggest that arousal-induced pupil dilation was mainly mediated by sympathetic activation, but pupil dilation related to saccade preparation was primarily mediated by parasympathetic inhibition.

Separate and overlapping functional roles for efference copies in the human thalamus.

How the perception of space is generated from the multiple maps in the brain is still an unsolved mystery in neuroscience. A neural pathway ascending from the superior colliculus through the medio-dorsal (MD) nucleus of thalamus to the frontal eye field has been identified in monkeys that conveys efference copy information about the metrics of upcoming eye movements. Information sent through this pathway stabilizes vision across saccades. We investigated whether this motor plan information might also shape spatial perception even when no saccades are performed. We studied patients with medial or lateral thalamic lesions (likely involving either the MD or the ventrolateral (VL) nuclei). Patients performed a double-step task testing motor updating, a trans-saccadic localization task testing visual updating, and a localization task during fixation testing a general role of motor signals for visual space in the absence of eye movements. Single patients with medial or lateral thalamic lesions showed deficits in the double-step task, reflecting insufficient transfer of efference copy. However, only a patient with a medial lesion showed impaired performance in the trans-saccadic localization task, suggesting that different types of efference copies contribute to motor and visual updating. During fixation, the MD patient localized stationary stimuli more accurately than healthy controls, suggesting that patients compensate the deficit in visual prediction of saccades - induced by the thalamic lesion - by relying on stationary visual references. We conclude that partially separable efference copy signals contribute to motor and visual stability in company of purely visual signals that are equally effective in supporting trans-saccadic perception.

Contributions to the study of spinocerebellar ataxia type 38 (SCA38).

OBJECTIVE: To report clinical and ancillary findings in a kindred with spinocerebellar ataxia 38 (SCA38). PATIENTS AND METHODS: Five family members spanning two generations developed gait ataxia and intermittent diplopia. On examination, a cerebellar syndrome accompanied by downbeat nystagmus and a saccadic head impulse test (HIT) were found. RESULTS: Whole-exome sequencing demonstrated a heterozygous variant in ELOVL5, c.779A > G (p.Tyr260Cys), in four tested patients. Intermittent concomitant esotropia and hypertropia caused transient diplopia in one individual each. Saccadic HIT responses were found in four subjects. Sensorineural hypoacusis was present in every case. Electrophysiological studies demonstrated a sensory neuronopathy in patients from the first generation, with prolonged disease duration. Baseline serum docosahexaenoic acid (DHA) percent was diminished in four individuals. Oral 26-week dietary DHA supplementation, 650 mg/day, raised serum DHA percent and induced a statistically significant reduction in Scale for the Assessment and Rating of Ataxia (SARA) total scores, and in stance and heel-shin slide item scores. CONCLUSION: The mentioned ELOVL5 variant segregated with disease in this kindred. Downbeat nystagmus, intermittent heterotropia causing transient diplopia, vestibular impairment demonstrated by abnormal HIT, and sensory neuronopathy were part of the clinical picture in this series. DHA supplementation raised serum DHA percent in cases with diminished levels, and induced a clinical amelioration and a statistically significant reduction in SARA scores in the study group. Further studies are needed to investigate the role of these findings in SCA38, and to determine the response to prolonged DHA supplementation.

The Color Nutrition Information Paradox: Effects of Suggested Sugar Content on Food Cue Reactivity in Healthy Young Women.

Color nutrition information (CNI) based on a traffic light system conveys information about food quality with a glance. The color red typically indicates detrimental food characteristics (e.g., very high sugar content) and aims at inhibiting food shopping and consumption. Red may, however, also elicit cross-modal associations with sweet taste, which is a preferable food characteristic. We conducted two experiments. An eye-tracking study investigated whether CNI has an effect on cue reactivity (dwell time, saccadic latency, wanting/liking) for sweet foods. The participants were presented with images depicting sweets (e.g., cake). Each image was preceded by a colored circle that informed about the sugar content of the food (red = high, green = low, gray = unknown). It was tested whether the red circle would help the participants to direct their gaze away from the 'high sugar' item. A second experiment investigated whether colored prime circles (red, green, gray) without nutrition information would influence the assumed sweetness of a food. In Experiment 1, CNI had the opposite of the intended effect. Dwell time and saccadic latency were higher for food items preceded by a red compared to a green circle. This unintended response was positively associated with participants' liking of sweet foods. CNI did not change the wanting/liking of the displayed foods. In Experiment 2, we found no evidence for color priming on the assumed sweetness of food. Our results question whether CNI is helpful to influence initial cue reactivity toward sweet foods.

Evidence for the world as an external memory: A trade-off between internal and external visual memory storage.

We use visual working memory (VWM) to maintain the visual features of objects in our world. Although the capacity of VWM is limited, it is unlikely that this limit will pose a problem in daily life, as visual information can be supplemented with input from our external visual world by using eye movements. In the current study, we influenced the trade-off between eye movements and VWM utilization by introducing a cost to a saccade. Higher costs were created by adding a delay in stimulus availability to a copying task. We show that increased saccade cost results in less saccades towards the model and an increased dwell time on the model. These results suggest a shift from making eye movements towards taxing internal VWM. Our findings reveal that the trade-off between executing eye-movements and building an internal representation of our world is based on an adaptive mechanism, governed by cost-efficiency.

Alpha Oscillations in the Human Brain Implement Distractor Suppression Independent of Target Selection.

In principle, selective attention is the net result of target selection and distractor suppression. The way in which both mechanisms are implemented neurally has remained contested. Neural oscillatory power in the alpha frequency band (∼10 Hz) has been implicated in the selection of to-be-attended targets, but there is lack of empirical evidence for its involvement in the suppression of to-be-ignored distractors. Here, we use electroencephalography recordings of N = 33 human participants (males and females) to test the preregistered hypothesis that alpha power directly relates to distractor suppression and thus operates independently from target selection. In an auditory spatial pitch discrimination task, we modulated the location (left vs right) of either a target or a distractor tone sequence, while fixing the other in the front. When the distractor was fixed in the front, alpha power relatively decreased contralaterally to the target and increased ipsilaterally. Most importantly, when the target was fixed in the front, alpha lateralization reversed in direction for the suppression of distractors on the left versus right. These data show that target-selection-independent alpha power modulation is involved in distractor suppression. Although both lateralized alpha responses for selection and for suppression proved reliable, they were uncorrelated and distractor-related alpha power emerged from more anterior, frontal cortical regions. Lending functional significance to suppression-related alpha oscillations, alpha lateralization at the individual, single-trial level was predictive of behavioral accuracy. These results fuel a renewed look at neurobiological accounts of selection-independent suppressive filtering in attention.SIGNIFICANCE STATEMENT Although well established models of attention rest on the assumption that irrelevant sensory information is filtered out, the neural implementation of such a filter mechanism is unclear. Using an auditory attention task that decouples target selection from distractor suppression, we demonstrate that two sign-reversed lateralized alpha responses reflect target selection versus distractor suppression. Critically, these alpha responses are reliable, independent of each other, and generated in more anterior, frontal regions for suppression versus selection. Prediction of single-trial task performance from alpha modulation after stimulus onset agrees with the view that alpha modulation bears direct functional relevance as a neural implementation of attention. Results demonstrate that the neurobiological foundation of attention implies a selection-independent alpha oscillatory mechanism to suppress distraction.

Task-based fMRI of a free-viewing visuo-saccadic network in the marmoset monkey.

Saccadic tasks are often used to index aberrations of cognitive function in patient populations, with several neuropsychiatric and neurologic disorders characterized by saccadic dysfunction. The common marmoset (Callithrix jacchus) has received recent attention as an additional primate model for studying the neural basis of these dysfunctions - marmosets are amenable to a host of genetic manipulation techniques and have a lissencephalic cortex, which is well suited for a variety of recording techniques (e.g., calcium imaging, laminar electrophysiology). Because the marmoset cortex is mostly lissencephalic, however, the locations of frontal saccade-related regions (e.g., frontal eye fields (FEF)) are less readily identified than in Old World macaque monkeys. Further, although high quality histology-based atlases do exist for marmosets, identifying these regions based on histology alone is not always accurate, with the cytoarchitectonic boundaries often inconsonant with functional boundaries. As such, there is a need to map the functional location of these regions directly. Task-based functional magnetic resonance imaging (fMRI) is of utility in this regard, allowing for detection of whole-brain signal changes in response to moving stimuli. Here, we conducted task-based fMRI in marmosets at ultra-high field (9.4 T) during a free-viewing visuo-saccadic task. We also conducted the same task in humans at ultra-high field (7 T) to validate that our simple task was indeed evoking the visuo-saccadic circuitry we expected (as defined by a meta-analysis of fMRI saccade studies). In the marmosets, we found that the task evoked a robust visuo-saccadic topology, with visual cortex (V1, V2, V3, V4) activation extending ventrally to MT, MST, FST and dorsally into V6, 19M, 23V. This topology also included putative cingulate eye field (area 32 and 24d), posterior parietal cortex (with strongest activation in lateral intraparietal area (LIP)), and a frontolateral peak in area 8 aV in marmosets, extending into 45, 46, 8aD, 6DR, 8c, 6 aV, 6DC. Overall, these results support the view that marmosets are a promising preclinical modelling species for studying saccadic dysfunction related to neuropsychiatric or neurodegenerative human brain diseases.

Eye movement desensitization and reprocessing for post-traumatic stress disorder from the perspective of three-dimensional model of the experiential selfhood.

Eye Movement Desensitization and Reprocessing (EMDR) therapy is included in many international trauma treatment guidelines and is also shortlisted as an evidence-based practice for the treatment of psychological trauma and Post-Traumatic Stress Disorder (PTSD). However, its neurobiological mechanisms have not yet been fully understood. In this brief article we propose a hypothesis that a recently introduced neurophysiologically based three-dimensional construct model for experiential selfhood may help to fill this gap by providing the necessary neurobiological rationale of EMDR. In support of this proposal we briefly overview the neurophysiology of eye movements and the triad selfhood components, as well as EMDR therapy neuroimaging studies.

Eye tracker outcomes in a randomized trial of 40 sessions of hyperbaric oxygen or sham in participants with persistent post concussive symptoms.

PURPOSE: Eye movements may offer a sensitive method to measure response to intervention in mild traumatic brain injury (mTBI). METHODS: The Brain Injury and Mechanisms of Action of Hyperbaric Oxygen for Persistent Post-Concussive Symptoms after Mild Traumatic Brain Injury Study (BIMA) randomized 71 participants to 40 sessions of hyperbaric oxygen or sham. A companion normative study (Normal) enrolled 75 participants. An eye tracking system measured left and right eye movements for saccadic and smooth pursuit. At baseline two smooth pursuit tasks, circular and horizontal ramp, and four saccadic tasks, horizontal and vertical step, reading, and memory guided-on tasks differentiated BIMA from Normal participants. The change from baseline in these tasks were measured and compared between interventions and against Normal participants at 13 weeks and six-month follow-up using the two-sample t-test. The Holm-Bonferroni procedure was used to adjust for multiple testing. RESULTS: Change from baseline in eyetracker measures for participants assigned to the hyperbaric oxygen arm did not significantly differ from those assigned to the sham arm at post-randomization time points 13 weeks and six months. Consistent shifts of BIMA participant values toward Normal values at 13 weeks and six months were observed for overall fixation duration, forward saccadic duration, and number of lines read for the reading task, number of misses on the memory guided-on task, and absolute intersaccadic interval velocity and absolute saccadic amplitude on the circular task. The distributions between Normal and BIMA participants were no longer statistically significantly different at 13 weeks and six months post enrollment for these measures. CONCLUSION: The baseline differences between BIMA and Normal suggest potential vulnerability of the smooth pursuit system and the saccadic system. During the six-month follow-up period, improvement toward Normal was seen on some measures in both the hyperbaric oxygen and sham intervention arms without difference between intervention groups. IDS: clinicaltrials.gov Identifiers NCT01611194 and NCT01925963.

Peripheral Vision in Martial Arts Experts: The Cost-Dependent Anchoring of Gaze.

Research on martial arts has suggested that gaze anchoring is functional for optimizing the use of peripheral visual information. The current study predicted that the height of gaze anchoring on the opponent's body would depend on the potential attacking locations that need to be monitored. To test this prediction, the authors compared high-level athletes in kung fu (Qwan Ki Do), who attack with their arms and legs, with Tae Kwon Do fighters, who attack mostly with their legs. As predicted, the results show that Qwan Ki Do athletes anchor their gaze higher than Tae Kwon Do athletes do before and even during the first attack. In addition, gaze anchoring seems to depend on 3 factors: the particulars of the evolving situation, crucial cues, and specific visual costs (especially suppressed information pickup during saccades). These 3 factors should be considered in future studies on gaze behavior in sports to find the most functional, that is, cost-benefit-optimized, gaze pattern.

Alterations in intrinsic fronto-thalamo-parietal connectivity are associated with cognitive control deficits in psychotic disorders.

Despite a growing number of reports about alterations in intrinsic/resting brain activity observed in patients with psychotic disorders, their relevance to well-established cognitive control deficits in this patient group is not well understood. Totally 88 clinically stabilized patients with a psychotic disorder and 50 healthy controls participated in a resting-state magnetic resonance imaging study (rs-MRI) and performed an antisaccade task in the laboratory to assess voluntary inhibitory control ability. Deficits on this task are a well-established biomarker across psychotic disorders as we found in the present patient sample. First, regional cerebral function was evaluated by measuring the amplitude of low frequency fluctuations (ALFF) in rs-MRI BOLD signals. We found reduced ALFF in patients in regions known to be relevant to antisaccade task performance including bilateral frontal eye fields (FEF), supplementary eye fields (SEF) and thalamus. Second, areas with ALFF alterations were used as seed areas in whole-brain functional connectivity (FC) analysis. Altered FC was observed in a fronto-thalamo-parietal network that was associated with inhibition error rate in patients but not in controls. In contrast, faster time to generate a correct antisaccade was associated with FC in FEF and SEF in controls but this effect was not seen in patients. These findings establish a behavioral relevance of resting-state fMRI findings in psychotic disorders, and extend previous reports of alterations in fronto-thalamo-parietal network activation during antisaccade performance seen in task-based fMRI studies.

Distraction by deviant sounds during reading: An eye-movement study.

Oddball studies have shown that sounds unexpectedly deviating from an otherwise repeated sequence capture attention away from the task at hand. While such distraction is typically regarded as potentially important in everyday life, previous work has so far not examined how deviant sounds affect performance on more complex daily tasks. In this study, we developed a new method to examine whether deviant sounds can disrupt reading performance by recording participants' eye movements. Participants read single sentences in silence and while listening to task-irrelevant sounds. In the latter condition, a 50-ms sound was played contingent on the fixation of five target words in the sentence. On most occasions, the same tone was presented (standard sound), whereas on rare and unexpected occasions it was replaced by white noise (deviant sound). The deviant sound resulted in significantly longer fixation durations on the target words relative to the standard sound. A time-course analysis showed that the deviant sound began to affect fixation durations around 180 ms after fixation onset. Furthermore, deviance distraction was not modulated by the lexical frequency of target words. In summary, fixation durations on the target words were longer immediately after the presentation of the deviant sound, but there was no evidence that it interfered with the lexical processing of these words. The present results are in line with the recent proposition that deviant sounds yield a temporary motor suppression and suggest that deviant sounds likely inhibit the programming of the next saccade.

In vivo manganese tract tracing of frontal eye fields in rhesus macaques with ultra-high field MRI: Comparison with DWI tractography.

The saccadic eye movement system has emerged as a valuable model for studying neural circuitry related to flexible control of behavior. Although connections of the saccadic circuitry are well documented via histochemical tracers, these methods require fixed tissue and thus cannot provide longitudinal assessments of connectivity. To circumvent this, diffusion weighted imaging (DWI) is often used as a proxy for connectivity in vivo, allowing for the tracing of connections longitudinally and noninvasively. DWI, however, has certain limitations in its ability to estimate the paths of fiber tracts. Here, we demonstrate the use of manganese, in an animal model, as an MRI-based in vivo labeling technique for saccadic circuitry that allows for direct tract tracing without the need to sacrifice the animal. Manganese is a strong paramagnetic contrast agent used for T1-relaxation enhancement in MRI. Here, we locally injected MnCl2 into the frontal eye fields (FEF), a key saccadic node, of two male rhesus macaques and collected ultra-high field MRI data at 7 T (T1, DWI). The results demonstrate that MnCl2-traced FEF connections parallel those established by histochemical tracing (albeit at a lower spatial resolution) and suggest that DWI underestimates FEF connectivity, likely due to crossing fibers and small tract size. These results highlight the lack of DWI sensitivity for tracing subcortical FEF fibers, but also suggest MnCl2-based tracing as a powerful alternative for assessing these connections in vivo.

Arousal dependent modulation of thalamo-cortical functional interaction.

Ongoing changes in arousal influence sensory processing and behavioral performance. Yet the circuit-level correlates for this influence remain poorly understood. Here, we investigate how functional interaction between posterior parietal cortex (PPC) and lateral posterior (LP)/Pulvinar is influenced by ongoing fluctuations in pupil-linked arousal, which is a non-invasive measure of neuromodulatory tone in the brain. We find that fluctuations in pupil-linked arousal correlate with changes to PPC to LP/Pulvinar oscillatory interaction, with cortical alpha oscillations driving activity during low arousal states, and LP/Pulvinar driving PPC in the theta frequency band during higher arousal states. Active visual exploration by saccadic eye movements elicits similar transitions in thalamo-cortical interaction. Furthermore, the presentation of naturalistic video stimuli induces thalamo-cortical network states closely resembling epochs of high arousal in the absence of visual input. Thus, neuromodulators may play a role in dynamically sculpting the patterns of thalamo-cortical functional interaction that underlie visual processing.