The assessment of mental effort is increasingly relevant in neurocognitive and life span 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 ( n = 44) adults 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 neurocognitive 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).

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 this 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 BG, 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 BG. 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 Theory's assertion that eye movements both encode, and are themselves embedded in, mnemonic representations.

The ventromedial prefrontal cortex (vmPFC) is involved in diverse cognitive operations, from inhibitory control to processing of semantic schemas. When accompanied by damage to the basal forebrain, vmPFC lesions can also impair relational memory, the ability to form and recall relations among items. Impairments in establishing direct relations among items (e.g., A is related to B, B is related to C) can also hinder the transitive processing of indirect relationships (e.g., inferring that A and C are related through direct relations that each contain B). Past work has found that transitive inference improves when the direct relations are organized within an existing knowledge structure, or schema. This type of semantic support is most effective for individuals whose relational memory deficits are mild (e.g., healthy age-related decline) rather than pronounced (e.g., hippocampal amnesia, amnestic mild cognitive impairment). Given that vmPFC damage can produce both relational memory and schema processing deficits, such damage may pose a particular challenge in establishing the type of relational structure required for transitive inference, even when supported by preexisting knowledge. To examine this idea, we tested individuals with lesions to the mPFC on multiple conditions that varied in pre-experimental semantic support and explored the extent to which they could identify both previously studied (direct) and novel transitive (indirect) relations. Most of the mPFC cases showed marked transitive inference deficits and even showed impaired knowledge of preexisting, direct, semantic relations, consistent with disruptions to schema-related processes. However, one case with more dorsal mPFC damage showed preserved ability to identify direct relations and make novel inferences, particularly when pre-experimental knowledge could be used to support performance. These results suggest that damage to the mPFC and basal forebrain can impede establishment of ad hoc relational schemas upon which transitive inference is based, but that appealing to prior knowledge may still be useful for those neurological cases that have some degree of preserved relational memory.

The lateral portion of the entorhinal cortex is one of the first brain regions affected by tau pathology, an important biomarker for Alzheimer disease. Improving our understanding of this region's cognitive role may help identify better cognitive tests for early detection of Alzheimer disease. 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, L. K., Olsen, R. K., Bild-Enkin, H. E. P., D'Angelo, M. C., Kacollja, A., McQuiggan, D. A., et al. Anterolateral entorhinal cortex volume predicted by altered intra-item configural processing. Journal of Neuroscience , 37 , 5527–5538, 2017]. In this 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 eye-tracking 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, D. I., Langston, R. F., Schlesiger, M. I., Wagner, M., Watanabe, S., & Ainge, J. A. Lateral entorhinal cortex is critical for novel object-context recognition. Hippocampus , 23 , 352–366, 2013], and object-trace memory, the memory for the former location of objects [Tsao, A., Moser, M. B., & Moser, E. I. Traces of experience in the lateral entorhinal cortex. Current Biology , 23 , 399–405, 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 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.

Visual behavior is guided by memories from prior experience and knowledge of the visual scene. The hippocampal system (HC), in particular, has been implicated in the guidance of saccades: Amnesic patients, following damage to the HC, exhibit selective deficits in their gaze patterns. However, the neural circuitry by which mnemonic representations influence the oculomotor system remains unknown. We used a data-driven, network-based approach on directed anatomical connectivity from the macaque brain to reveal an extensive set of polysnaptic pathways spanning the extrastriate, posterior parietal and prefrontal cortices that potentially mediate the exchange of information between the memory and visuo-oculomotor systems. We additionally show how the potential for directed information flow from the hippocampus to oculomotor control areas is exceptionally high. In particular, the dorsolateral pFC and FEF—regions known to be responsible for the cognitive control of saccades—are topologically well positioned to receive information from the hippocampus. Together with neuropsychological evidence of altered gaze patterns following damage to the hippocampus, our findings suggest that a reconsideration of hippocampal involvement in oculomotor guidance is needed.

It is well known that previous perceptual experiences alter subsequent perception, but the details of the neural underpinnings of this general phenomenon are still sketchy. Here, we ask whether previous experiences with an item (such as seeing a person's face) leads to the alteration of the neural correlates related to processing of the item as such, or whether it creates additional associative connections between such substrates and those activated during prior experience. To address this question, we used magnetoencephalography (MEG) to identify neural changes accompanying subjects' viewing of unfamiliar versus famous faces and hearing the names of unfamiliar versus famous names. We were interested in the nature of the involvement of auditory brain regions in the viewing of faces, and in the involvement of visual regions in the hearing of names. Evoked responses from MEG recordings for the names and faces conditions were localized to auditory and visual cortices, respectively. Unsurprisingly, peak activation strength of evoked responses was larger for famous versus nonfamous names within the superior temporal gyrus (STG), and was similar for famous and nonfamous faces in the occipital cortex. More relevant to the issue of experience on perception, peak activation strength in the STG was larger for viewed famous versus nonfamous faces, and peak activation within the occipital cortex was larger for heard famous versus nonfamous names. Critically, these experience-related responses were present within 150–250 msec of stimulus onset. These findings support the hypothesis that prior experiences may influence processing of faces and names such that perception encompasses more than what is imparted on the senses.

Little is known about the mechanisms by which memory for relations is accomplished, or about the time course of the critical processes. Here, eye movement measures were used to examine the time course of subjects' access to and use of relational memory. In four experiments, participants studied faces superimposed on scenic backgrounds and were tested with three-face displays superimposed on the scenes viewed earlier. Participants exhibited disproportionate viewing of the face originally studied with the scene, compared to other equally familiar faces in the test display. When a preview of a previously viewed scene was provided, permitting expectancies about the to-be-presented face to emerge, disproportionate viewing was manifested within 500–750 msec after test display onset, more than a full second in advance of explicit behavioral responses, and occurred even when overt responses were not required. In the absence of preview, the viewing effects were delayed by approximately 1 sec. Relational memory effects were absent in the eye movement behavior of amnesic patients with hippocampal damage, suggesting that these effects depend critically on the hippocampal system. The results provide an index of memory for face-scene relations, indicate the time by which retrieval and identification of these relations occur, and suggest that retrieval and use of relational memory depends critically on the hippocampus and occurs obligatorily, regardless of response requirements.

Human and nonhuman animal research has outlined the neural regions that support saccadic eye movements. The aim of the current work was to outline the sequence by which distinct neural regions come on-line to support goal-directed saccade execution and error-related feedback. To achieve this, we obtained behavioral responses via eye movement recordings and neural responses via magnetoencephalography (MEG), concurrently, while participants performed an antisaccade task. Neural responses were examined with respect to the onset of the saccadic eye movements. Frontal eye field and visual cortex activity distinguished subsequently successful goal-directed saccades from (correct and erroneous) reflexive saccades prior to the deployment of the eye movement. Activity in the same neural regions following the saccadic movement distinguished correct from incorrect saccadic responses. Error-related activity in the frontal eye fields preceded that from visual regions, suggesting a potential feedback network that may drive corrective eye movements. This work provides the first empirical demonstration of simultaneous remote eyetracking and MEG recording. The coupling of behavioral and neuroimaging technologies, used here to characterize dynamic brain networks underlying saccade execution and error-related feedback, demonstrates a novel within-paradigm converging evidence approach by which to outline the neural underpinnings of cognition.