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Ryan, J. D.

Publications and source records attributed to Ryan, J. D..

12 recordsLinked to original sources

The Listening Effort Profile of Eye Movements: Easy, Difficult, and Impossible Speech Comprehension

Speech comprehension in noisy environments often requires cognitive effort, but listeners may disengage when comprehension becomes impossible. Eye movements have recently emerged as a promising new measure of listening effort, but it remains unclear whether eye movements are sensitive to the full effort profile across easy, difficult, and impossible speech comprehension. Across four experiments, participants listened to sentences at easy, difficult, and impossible levels of multi-talker background babble while pupil size and eye movements were recorded. Pupil size generally followed the expected inverted u-shaped effort profile: low for easy speech, maximal for difficult but still intelligible speech and lower again for impossible speech, although this pattern partly reflected sustained, condition-specific differences and not only sentence-evoked responses. Gaze dispersion - measuring the spread of eye movements - decreased with high temporal selectivity during difficult relative to easy and impossible speech, indicating reduced eye movements during active, effortful listening. However, gaze dispersion was also lower, but less temporally selective, during impossible compared to easy listening, especially in non-baseline-corrected analyses, suggesting that reduced eye movements do not index listening effort uniquely. Instead, eye movements appear to reflect both attentional engagement during difficult listening and disengagement or inward attention when meaningful listening is no longer possible. These findings indicate that pupil size and eye movements provide complementary indices of listening-related cognition, and highlight the integration of listening, cognition, and motor systems.

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Phase-locking saccades to posterior alpha oscillations improves the neural representation of visual objects during memory formation

Visual memory formation begins with the intake and neural processing of discrete samples provided by gaze fixations and saccades. Past research has highlighted a functional relationship between the timing of saccades and oscillations in neural activity over posterior brain areas: saccades phase-lock to alpha oscillations (8-12 Hz) and the degree of phase-locking, in natural scenes, has been associated with subsequent recognition memory. Here, we tested the hypothesis that the putative memory encoding benefit arises due to improved neuronal processing and, ultimately, better neural representation of foveated items, when saccades are locked to alpha phase. In a co-registered magnetoencephalography (MEG) and eye-tracking paradigm, participants executed saccades from central fixation to images that appeared in the periphery, attempting to remember those images for later testing. Replicating past results, saccades to subsequently remembered images were preceded by greater inter-trial phase coherence in the alpha frequency band, at posterior MEG channels, consistent with the notion that the eye movements were phase-locked. Across participants, the degree of saccade phase-locking was positively correlated with how well visual and semantic properties of the images were represented in neural activity, within 200 ms of their foveation. This relationship was evident in responses localized to the left parieto-occipital and ventral temporal cortex, where greater saccade phase-locking was associated with improved visual and semantic representations, respectively. These results support the hypothesis that phase-locking saccades to alpha oscillations leads to improved neuronal representation of foveated stimuli, providing new mechanistic insight into how episodic memories are formed from discrete visual samples. Significance StatementVisual memories begin with discrete samples provided by eye movements and gaze fixations, from which the brain must extract information that is integrated into a coherent memory trace. This work examined the neural mechanisms that support this memory formation process, one eye movement at a time. The results identified a functioning coupling between saccade timing and neuronal oscillations in the alpha frequency band: when saccades are phase-locked to alpha oscillations, the brain can better process the visual information provided by gaze fixations. This indicates that precise coordination of saccade timing, with respect to neuronal oscillations, promotes more veridical neural representation of the resulting visual samples, from which accurate episodic memories can be constructed.

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Effective connectivity between the medial temporal lobes and early visual cortex modulated by unrestricted viewing predicts memory retrieval and gaze reinstatement

Memory and gaze behavior are intricately linked, guiding one another to extract information and create mental representations of our environment for subsequent retrieval. Recent findings from functional neuroimaging and computational modeling suggest that reciprocal interactions between the extended hippocampal system and visuo-oculomotor regions are functionally relevant for building these mental representations during visual exploration. Yet, evidence for the directionality of information flow during encoding within this reciprocal architecture in humans is limited. In the current study, we used dynamic causal modeling (DCM) to give a non-invasive account for the directional influences between these systems when new memories are created. Here, we provide novel evidence demonstrating how unrestricted, naturalistic visual exploration induces changes in this connectivity. Subsequent memory retrieval performance was also predicted by the pattern of connectivity modulated by unrestricted visual exploration, identifying the mechanism underlying a rich history of previous work linking increased gaze behavior during encoding to later memory. Together, these findings suggest that gaze behavior shapes the ways in which brain dynamics within and between the hippocampal system and early visual cortex unfold during encoding in humans. Importantly, these directional interactions support the building of coherent, lasting mental representations.

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Remembrance with gazes passed: Eye movements precede continuous recall of episodic details of real-life events

Autobiographical memory entails reconstructing the visual features of past events. Eye movements are associated with vivid autobiographical recollection, but this research has yet to capitalize on the high temporal resolution of eye-tracking data. We aligned eye movement data with participants simultaneous free recall of a verified real-life event, allowing us to assess the temporal correspondence of saccades to production of episodic and non-episodic narrative content at the millisecond level. Eye movements reliably predicted subsequent episodic - but not non-episodic - details by 250-1100 ms, suggesting that they facilitate episodic recollection by reinstating spatiotemporal context during vivid recollection. Assessing the relationship of oculomotor responses to naturalistic memory informs theory as well as diagnosis and treatment of conditions involving pathological recollection, such as Alzheimers disease and post-traumatic stress disorder (PTSD).

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Pupil size and eye movements differently index effort in both younger and older adults

The assessment of mental effort is increasingly relevant in neuro-cognitive and lifespan domains. Pupillometry, the measure of the pupil size, is often used to assess effort but has disadvantages. Analysis of eye movements may provide an alternative, but research has been limited to easy and difficult task demands in younger adults. An effort measure must be sensitive to the whole effort profile, including giving up effort investment, and capture effort in different age groups. The current study comprised three experiments in which younger (N=66) and older adults (N=44) listened to speech masked by background babble at different signal-to-noise ratios associated with easy, difficult, and impossible speech comprehension. We expected individuals to invest little effort for easy and impossible speech ( giving up) but to exert effort for difficult speech. Indeed, pupil size was largest for difficult, but lower for easy and impossible speech. In contrast, gaze dispersion decreased with increasing speech masking in both age groups. Critically, gaze dispersion during difficult speech returned to levels similar to easy speech after sentence offset, when acoustic stimulation was similar across conditions, whereas gaze dispersion during impossible speech continued to be reduced. These findings show that a reduction in eye movements is not a byproduct of acoustic factors, but instead suggest that neuro-cognitive processes, different from arousal-related systems regulating the pupil size, drive reduced eye movements during high task demands. The current data thus show that effort in one sensory domain (audition) differentially impacts distinct functional properties in another sensory domain (vision). Significance statementThe assessment of mental effort is increasingly relevant in many domains. Here, we investigated the sensitivity of a novel measure of effort - the spatial dispersion of eye movements - and compared it to pupillometry, which is a more common effort-assessment tool. Individuals listened to speech masked by background babble at levels associated with easy, difficult, and impossible speech comprehension. Pupil size was largest for difficult, but lower for easy and impossible speech conditions (giving up listening). In contrast, the spatial dispersion of eye movements decreased with increasing speech masking, but this effect was independent of acoustic factors. Instead, the current results suggest that neuro-cognitive processes, different from arousal-related systems regulating the pupil size, drive reduced eye movements during high task demands.

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Unrestricted eye movements strengthen causal connectivity from hippocampal to oculomotor regions during scene construction

Scene construction is a key component of memory recall, navigation, and future imagining, and relies on the medial temporal lobes (MTL). A parallel body of work suggests that eye movements may enable the imagination and construction of scenes, even in the absence of external visual input. There are vast structural and functional connections between regions of the MTL and those of the oculomotor system. However, the directionality of connections between the MTL and oculomotor control regions, and how it relates to scene construction, has not been studied directly in human neuroimaging. In the current study, we used dynamic causal modeling (DCM) to interrogate effective connectivity between the MTL and oculomotor regions using a scene construction task in which participants eye movements were either restricted (fixed-viewing) or unrestricted (free-viewing). By omitting external visual input, and by contrasting free- versus fixed- viewing, the directionality of neural connectivity during scene construction could be determined. As opposed to when eye movements were restricted, allowing free viewing during construction of scenes strengthened top-down connections from the MTL to the frontal eye fields, and to lower-level cortical visual processing regions, suppressed bottom-up connections along the visual stream, and enhanced vividness of the constructed scenes. Taken together, these findings provide novel, non-invasive evidence for the causal architecture between the MTL memory system and oculomotor system associated with constructing vivid mental representations of scenes. HighlightsO_LIThe role of eye movements in mentally constructing scene imagery was investigated C_LIO_LIRestricting eye movements impaired vividness of constructed scene imagery C_LIO_LIMaking eye movements strengthened connectivity from memory to oculomotor regions C_LI

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Neural correlates of subsequent memory-related gaze reinstatement

Mounting evidence linking gaze reinstatement- the recapitulation of encoding-related gaze patterns during retrieval- to behavioral measures of memory suggests that eye movements play an important role in mnemonic processing. Yet, the nature of the gaze scanpath, including its informational content and neural correlates, has remained in question. In the present study, we examined eye movement and neural data from a recognition memory task to further elucidate the behavioral and neural bases of functional gaze reinstatement. Consistent with previous work, gaze reinstatement during retrieval of freely-viewed scene images was greater than chance and predictive of recognition memory performance. Gaze reinstatement was also associated with viewing of informationally salient image regions at encoding, suggesting that scanpaths may encode and contain high-level scene content. At the brain level, gaze reinstatement was predicted by encoding-related activity in the occipital pole and basal ganglia, neural regions associated with visual processing and oculomotor control. Finally, cross-voxel brain pattern similarity analysis revealed overlapping subsequent memory and subsequent gaze reinstatement modulation effects in the parahippocampal place area and hippocampus, in addition to the occipital pole and basal ganglia. Together, these findings suggest that encoding-related activity in brain regions associated with scene processing, oculomotor control, and memory supports the formation, and subsequent recapitulation, of functional scanpaths. More broadly, these findings lend support to Scanpath Theorys assertion that eye movements both encode, and are themselves embedded in, mnemonic representations.

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Restricting visual exploration directly impedes neural activity, functional connectivity, and memory.

We move our eyes to explore the visual world, extract information, and create memories. The number of gaze fixations - the stops that the eyes make - has been shown to correlate with activity in the hippocampus, a region critical for memory, and with later recognition memory. Here, we combined eyetracking with fMRI to provide direct evidence for the relationships between gaze fixations, neural activity, and memory during scene viewing. Compared to free viewing, fixating a single location reduced: 1) subsequent memory, 2) neural activity along the ventral visual stream into the hippocampus, 3) neural similarity between effects of subsequent memory and visual exploration, and 4) functional connectivity among the hippocampus, parahippocampal place area, and other cortical regions. Gaze fixations were uniquely related to hippocampal activity, even after controlling for neural effects due to subsequent memory. Individual gaze fixations may provide the basic unit of information on which memory binding processes operate.

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Eye movements support behavioral pattern completion

The ability to recall a detailed event from a simple reminder is supported by pattern completion, a cognitive operation performed by the hippocampus wherein existing mnemonic representations are retrieved from incomplete input. In behavioral studies, pattern completion is often inferred through the false endorsement of lure (i.e., similar) items as old. However, evidence that such a response is due to the specific retrieval of a similar, previously encoded item is severely lacking. We used eye movement (EM) monitoring during a partial-cue recognition memory task to index reinstatement of lure images behaviorally via the recapitulation of encoding-related EMs or, gaze reinstatement. Participants reinstated encoding-related EMs following degraded retrieval cues and this reinstatement was negatively correlated with accuracy for lure images, suggesting that retrieval of existing representations (i.e., pattern completion) underlies lure false alarms. Our findings provide novel evidence linking gaze reinstatement and pattern completion and advance a functional role for EMs in memory retrieval.

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Object-in-Place Memory Predicted by Anterolateral Entorhinal Cortex and Parahippocampal Cortex Volume in Older Adults

The lateral portion of the entorhinal cortex is one of the first brain regions affected by tau pathology, an important biomarker for Alzheimers disease (AD). Improving our understanding of this regions cognitive role may help identify better cognitive tests for early detection of AD. Based on its functional connections, we tested the idea that the human anterolateral entorhinal cortex (alERC) may play a role in integrating spatial information into object representations. We recently demonstrated that the volume of the alERC was related to processing the spatial relationships of the features within an object (Yeung et al., 2017). In the present study, we investigated whether the human alERC might also play a role in processing the spatial relationships between an object and its environment using an eyetracking task that assessed visual fixations to a critical object within a scene. Guided by rodent work, we measured both object-in-place memory, the association of an object with a given context (Wilson et al., 2013), and object-trace memory, the memory for the former location of objects (Tsao, Moser, & Moser, 2013). In a group of older adults with varying stages of brain atrophy and cognitive decline, we found that the volume of the alERC and the volume of the parahippocampal cortex (PHC) selectively predicted object-in-place memory, but not object-trace memory. These results provide support for the notion that the alERC may integrate spatial information into object representations.

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The functional reach of the hippocampal memory system to the oculomotor system.

Visual exploration is related to activity in the hippocampus (HC) and/or extended medial temporal lobe system (MTL), is influenced by stored memories, and is altered in amnesic cases. An extensive set of polysynaptic connections exists both within and between the HC and oculomotor systems such that investigating how HC responses ultimately influence neural activity in the oculomotor system, and the timing by which such neural modulation could occur is not trivial. We leveraged TheVirtualBrain, a software platform for large-scale network simulations, to model the functional dynamics that govern the interactions between the two systems in the macaque cortex. Evoked responses following the stimulation of the MTL and some, but not all, subfields of the HC resulted in observable responses in oculomotor regions, including the frontal eye fields (FEF), within the time of a gaze fixation. Modeled lesions to some MTL regions slowed the dissipation of HC signal to oculomotor regions, whereas HC lesions generally did not affect the rapid MTL activity propagation to oculomotor regions. These findings provide a framework for investigating how information represented by the HC/MTL may influence the oculomotor system during a fixation and predict how HC lesions may affect visual exploration. Author SummaryNo major account of oculomotor (eye movement) guidance considers the influence of the hippocampus (HC) and broader medial temporal lobe (MTL) system, yet it is clear that information is exchanged between the two systems. Prior experience influences current viewing, and cases of amnesia due to compromised HC/MTL function show specific alterations in viewing behaviour. By modeling large-scale network dynamics, we show that stimulation of subregions of the HC, and of the MTL, rapidly results in observable responses in oculomotor control regions, and that HC/MTL lesions alter signal propagation. These findings suggest that information from memory may readily guide visual exploration, and calls for a reconsideration of the neural circuitry involved in oculomotor guidance.

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Eye-Movement Reinstatement and Neural Reactivation: Testing the Hebbian Theory of Mental Imagery

Half a century ago, Donald Hebb posited that mental imagery is a constructive process that emulates perception. Specifically, Hebb claimed that visual imagery results from the reactivation of neural activity associated with viewing images. He also argued that neural reactivation and imagery benefit from the re-enactment of eye movement patterns that first occurred at viewing (fixation reinstatement). To investigate these claims, we applied multivariate pattern analyses to functional MRI (fMRI) and eye-tracking data collected while healthy human participants repeatedly viewed and visualized complex images. We observed that the specificity of neural reactivation correlated positively with vivid imagery and with memory for stimulus image details. Moreover, neural reactivation correlated positively with fixation reinstatement, meaning that image-specific eye movements accompanied image-specific patterns of brain activity during visualization. These findings support the conception of mental imagery as a simulation of perception, and provide evidence of the supportive role of eye-movement in neural reactivation.

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