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Robertson, C. E.

Publications and source records attributed to Robertson, C. E..

13 recordsLinked to original sources

Hippocampal theta distinguishes between memory-guided and exploratory saccades in humans

Memory shapes how we explore the visual world, but the neural mechanisms linking mnemonic processes to eye movements during naturalistic viewing are not well understood. Theta-band oscillatory activity in the hippocampus is time-locked with eye movements in primates, suggesting a putative mechanism for coordinating mnemonic processing and oculomotor behaviour. Yet, it remains unknown whether this coupling generalises to episodic memory-guided viewing in humans, whether slow (3-6 Hz) and fast (6-10 Hz) theta bands play dissociable functions, and whether this coupling is sensitive to the direction of upcoming eye movements. Here, we used intracranial EEG and eye-tracking data from 11 neurosurgical patients of either sex (Keles et al., 2024) to address these questions. Using fixation-locked analyses, we found that hippocampal theta dynamics differentiate memory-guided from memory-independent fixations of episodically encoded naturalistic scenes (i.e., movies) through power and coherence mechanisms that are both temporally and spectrally dissociable. First, immediately after fixations ([~]0 to 250 ms), slow-theta power was more strongly suppressed during memory-guided trials (i.e., true positive, TP) than correct memory-independent trials (i.e., true negative, TN). Second, in the period around fixations (-80 to 60 ms), theta phase coherence increased independent of power during TP vs TN trials. This increase in coherence was most pronounced for contraversive relative to ipsiversive fixations, consistent with direction-sensitive hippocampal-oculomotor coordination during memory-guided viewing. Together, these findings suggest that hippocampal theta plays dissociable, time-locked roles in memory-guided fixations during naturalistic visual retrieval, supporting an ecologically relevant role for the hippocampus in coordinating memory and active visual behaviour. Significance statementMemory influences how we sample the visual environment, but the brain signals that link memory systems to eye movements are poorly understood. Using intracranial recordings from the human hippocampus during visual exploration of naturalistically encoded scenes, we demonstrate that theta-band activity differentiates memory-guided from memory-independent fixations in two ways: increased theta synchrony around fixation onset and reduced theta power modulations after fixation onset. These results reveal novel insights into how hippocampal theta helps coordinate memory-guided visual exploration.

neuroscience↗

Topography of scene memory and perception activity in posterior cortex - a publicly available resource

Adaptive behavior in complex environments requires integrating visual perception with memory of our spatial environment. Recent work has implicated three brain areas in posterior cerebral cortex -- the place memory areas (PMAs) that are anterior to the three visual scene perception areas (SPAs) - in this function. However, PMAs relationship to the broader cortical hierarchy remains unclear due to limited group-level characterization. Here, we examined the PMA and SPA locations across three fMRI datasets (44 participants, 29 female). SPAs were identified using a standard visual localizer where participants viewed scenes versus faces. PMAs were identified by contrasting activity when participants recalled personally familiar places versus familiar faces (Datasets 1-2) or places versus multiple categories (familiar faces, bodies, and objects, and famous faces; Dataset 3). Across datasets, the PMAs were located anterior to the SPAs on the ventral and lateral cortical surfaces. The anterior displacement between PMAs and SPAs was highly reproducible. Compared to public atlases, the PMAs fell at the boundary between externally-oriented networks (dorsal attention) and internally-oriented networks (default mode). Additionally, while SPAs overlapped with retinotopic maps, the PMAs were consistently located anterior to mapped visual cortex. These results establish the anatomical position of the PMAs at inflection points along the cortical hierarchy between unimodal sensory and transmodal, apical regions, which informs broader theories of how the brain integrates perception and memory for scenes. We have released probabilistic parcels of these regions to facilitate future research into their roles in spatial cognition. Significance statementComplex behavior requires the dynamic interplay between mnemonic and perceptual information. For example, navigation requires representation of the current visual scene and its relationship to the surrounding visuospatial context. We have suggested that the place memory areas, three brain areas located anterior to the scene perception areas in visual cortex, are well-positioned to serve this role. Here, in a large group of participants, we show that the place memory areas are robustly localizable, and that their position at the interface of multiple distributed brain networks is uniquely suited to mnemonic-perceptual integration. We have released probabilistic regions-of-interest and localization procedure so that others can identify these areas in their own participants.

neuroscience↗

Network-based representation learning reveals the impact of time and diet on the gut microbial and metabolomic environment of infants

BackgroundWhile studies have explored differences in gut microbiome development for infant liquid diets (breastmilk, formula), little is known about the impact of complementary foods on infant gut microbiome development. Here, we investigated how different protein-rich foods (i.e., meat vs. dairy) affect fecal metagenomics and metabolomics during early complementary feeding from 5-12 months in U.S. formula-fed infants from a randomized controlled feeding trial. ResultsWe used a novel network representation learning approach to model the time-dependent, complex interactions between microbiome features, metabolite compounds, and diet. We then used the embedded space to detect features associated with age and diet type and found the meat diet group was enriched with microbial genes encoding amino acid, nucleic acid, and carbohydrate metabolism. Compared to a more traditional differential abundance analysis, which analyzes features independently and found no significant diet associations, network node embedding represents the infant samples, microbiome features, and metabolites in a single transformed space revealing otherwise undetected associations between infant diet and the gut microbiome. ConclusionsOur findings generate new hypotheses regarding the interplay between complementary feeding practices, microbial-metabolic interactions, and infant physiological outcomes. This work highlights the impact of complementary foods on infant gut microbiome development and the potential of using network representation learning to integrate multi-omic data, allowing for greater insight into complex diet, microbial, and metabolite interactions.

microbiology↗

Retinotopic coding organizes the opponent dynamic between internally and externally oriented brain networks

The human brain seamlessly integrates internally generated thoughts with incoming sensory information, yet the large-scale networks that support these functions -- the (Default Network, DN) and external (Dorsal Attention Network, dATN) -- are traditionally viewed as functionally independent. This raises a crucial question: how does the brain integrate information across these seemingly non-interactive systems? Here, using densely sampled 7T fMRI, individualized resting-state parcellations, and voxel-wise population-receptive-field mapping, we show that these internal/external networks are more interlocked than previously thought. Spontaneous DN and dATN activity during rest is uncorrelated at the network level. However, voxel-scale functional coupling across networks is shaped by the latent visual field preferences of individual voxels in each network, as measured during independent retinotopic mapping. Voxels that share visual field preferences exhibit stronger spontaneous coupling than those with divergent preferences. These retinotopically-specific interactions are bivalent: DN voxels with negative (suppressive) visual response amplitudes are anticorrelated with matched (positive) dATN voxels, while those DN voxels with positive response amplitudes are positively correlated. Thus, distinct subpopulations of visually-tuned DN voxels participate in spatially-specific interactions with the dATN. Further, retinotopic coding is intrinsic to the DN, persisting even during periods when the DN signal is elevated. These findings reveal a latent, voxel-level architecture of retinotopically-grounded interactions between the DN and dATN. Taken together, our results suggest that retinotopic coding underpins the dynamic coordination of perception and thought in the human brain.

neuroscience↗

Positive and Negative Retinotopic Codes in the Human Hippocampus

The hippocampus sits at the apex of the visual hierarchy, yet little is known about the visual properties of this core memory structure. Recent work suggests that a latent, bivalent retinotopic code persists in large-scale memory networks at the cortical apex, scaffolding interactions with sensory networks. Here, we tested whether a bivalent retinotopic code also persists within the hippocampus. To do this, we leveraged high-resolution 7T functional MRI along with voxel-scale visual population receptive field (pRF) modeling in 7 densely-sampled individuals (5 female). Our findings reveal a robust, voxel-scale retinotopic code broadly distributed across subfields and along the long axis of the human hippocampus, comprised of roughly equal proportions of pRFs with positive and negative amplitude responses to visual stimulation. Hippocampal pRFs displayed canonical visual properties, including stable valence and visual field preferences across runs and a contralateral bias. Retinotopic structure also persisted at rest: hippocampal voxels with similar pRF locations were more strongly correlated than voxels representing different visual field locations. Finally, across the ventral visual stream, the prevalence of negative-amplitude pRFs increased with mnemonic involvement, culminating in the balanced, bivalent organization within the hippocampus. These findings support the view that sensory and mnemonic systems are coupled through a shared retinotopic code at the apex of the visual hierarchy. Significance StatementThe hippocampus is closely coupled to the visual system, and recent work has challenged the classical view that visual coding schemes, like retinotopy, do not persist into the hippocampus. Here, we use high-resolution precision fMRI to robustly characterize a bivalent retinotopic code in the human hippocampus, consisting of both typical positive and atypical negative responses. We further show that this code predicts functional connectivity within the hippocampus even during non-visual tasks, suggesting that this bivalent retinotopic code may reflect an intrinsic organizational principle of the hippocampus relevant for perceptual-mnemonic segregation and integration.

neuroscience↗

A retinotopic code structures the interaction between perception and memory systems

Conventional views of brain organization suggest that the cortical apex processes internally-oriented information using an abstract, amodal neural code. Yet, recent reports have described the presence of retinotopic coding at the cortical apex, including the default mode network. What is the functional role of retinotopic coding atop the cortical hierarchy? Here, we report that retinotopic coding structures interactions between internally-oriented (mnemonic) and externally-oriented (perceptual) brain areas. Using fMRI, we observed robust, inverted (negative) retinotopic coding in category-selective memory areas at the cortical apex, which is functionally linked to the classic (positive) retinotopic coding in category-selective perceptual areas in high-level visual cortex. Specifically, these functionally-linked retinotopic populations in mnemonic and perceptual areas exhibit spatially-specific opponent responses during both bottom-up perception and top-down recall, suggesting that these areas are interlocked in a mutually-inhibitory dynamic. Together, these results show that retinotopic coding structures interactions between perceptual and mnemonic neural systems, thereby scaffolding their dynamic interaction.

neuroscience↗

Scene perception and visuospatial memory converge at the anterior edge of visually-responsive cortex

To fluidly engage with the world, our brains must simultaneously represent both the scene in front of us and our memory of the immediate surrounding environment (i.e., local visuospatial context). How does the brains functional architecture enable sensory and mnemonic representations to closely interface, while also avoiding sensory-mnemonic interference? Here, we asked this question using first-person, head-mounted virtual reality (VR) and fMRI. Using VR, human participants of both sexes learned a set of immersive, real-world visuospatial environments in which we systematically manipulated the extent of visuospatial context associated with a scene image in memory across three learning conditions, spanning from a single field-of-view to a city street. We used individualized, within-subject fMRI to determine which brain areas support memory of the visuospatial context associated with a scene during recall (Exp. 1) and recognition (Exp. 2). Across the whole brain, activity in three patches of cortex was modulated by the amount of known visuospatial context, each located immediately anterior to one of the three scene perception areas of high-level visual cortex. Individual subject analyses revealed that these anterior patches corresponded to three functionally-defined place memory areas, which selectively respond when visually recalling personally familiar places. In addition to showing activity levels that were modulated by the amount of visuospatial context, multivariate analyses showed that these anterior areas represented the identity of the specific environment being recalled. Together, these results suggest a convergence zone for scene perception and memory of the local visuospatial context at the anterior edge of high-level visual cortex. Significance statementAs we move through the world, the visual scene around us is integrated with our memory of the wider visuospatial context. Here, we sought to understand how the functional architecture of the brain enables coexisting representations of the current visual scene and memory of the surrounding environment. Using a combination of immersive virtual reality and fMRI, we show that memory of visuospatial context outside the current field-of-view is represented in a distinct set of brain areas immediately anterior and adjacent to the perceptually-oriented scene-selective areas of high-level visual cortex. This functional architecture would allow efficient interaction between immediately adjacent mnemonic and perceptual areas, while also minimizing mnemonic-perceptual interference.

neuroscience↗

Evaluating the efficacy of multi-echo ICA denoising on model-based fMRI

fMRI is an indispensable tool for neuroscience investigation, but this technique is limited by multiple sources of physiological and measurement noise. These noise sources are particularly problematic for analysis techniques that require high signal-to-noise ratio for stable model fitting, such as voxel-wise modeling. Multi-echo data acquisition in combination with echo-time dependent ICA denoising (ME-ICA) represents one promising strategy to mitigate physiological and hardware-related noise sources as well as motion-related artifacts. However, most studies employing ME-ICA to date are resting-state fMRI studies, and therefore we have a limited understanding of the impact of ME-ICA on task or model-based fMRI paradigms. Here, we addressed this knowledge gap by comparing data quality and model fitting performance on data acquired during a visual population receptive field (pRF) mapping paradigm (N=13 participants) after using one of three preprocessing procedures: ME-ICA, optimally combined multi-echo data without ICA-denoising, and typical single echo processing. As expected, multi-echo fMRI improved temporal signal-to-noise compared to single echo fMRI, with ME-ICA amplifying the improvement compared to optimal combination alone. However, unexpectedly, this boost in temporal signal-to-noise did not directly translate to improved model fitting performance: compared to single echo acquisition, model fitting was only improved after ICA-denoising. Specifically, compared to single echo acquisition, ME-ICA resulted in improved variance explained by our pRF model throughout the visual system, including anterior regions of the temporal and parietal lobes where SNR is typically low, while optimal combination without ICA did not. ME-ICA also improved reliability of parameter estimates compared to single echo and optimally combined multi-echo data without ICA-denoising. Collectively, these results suggest that ME-ICA is effective for denoising task-based fMRI data for modeling analyses and maintains the integrity of the original data. Therefore, ME-ICA may be beneficial for complex fMRI experiments, including task fMRI studies, voxel-wise modeling, and naturalistic paradigms.

neuroscience↗

Individual differences in visual search performance extend from artificial arrays to naturalistic environments.

Visual search is a universal human activity in naturalistic environments. Traditionally, visual search is investigated under tightly controlled conditions, where head-restricted participants locate a minimalistic target in a cluttered array presented on a computer screen. Do classic findings of visual search extend to naturalistic settings, where participants actively explore complex, real-world scenes? Here, we leverage advances in virtual reality (VR) technology to relate individual differences in classic visual search paradigms to naturalistic search behavior. In a naturalistic visual search task, participants looked for an object within their environment via a combination of head-turns and eye-movements using a head-mounted display. Then, in a classic visual search task, participants searched for a target within a simple array of colored letters using only eye-movements. We tested how set size, a property known to limit visual search within computer displays, predicts the efficiency of search behavior inside immersive, real-world scenes that vary in levels of visual clutter. We found that participants search performance was impacted by the level of visual clutter within real-world scenes. Critically, we also observed that individual differences in vi1-3sual search efficiency in classic search predicted efficiency in real-world search, but only when the comparison was limited to the forward-facing field of view for real-world search. These results demonstrate that set size is a reliable predictor of individual performance across computer-based and active, real-world visual search behavior.

neuroscience↗

A causal study of bumetanide on a marker of excitatory-inhibitory balance in the human brain

Bumetanide has received much interest as a potential pharmacological modulator of the putative imbalance in excitatory/inhibitory (E/I) signaling that is thought to characterize autism spectrum conditions. Yet, currently, no studies of bumetanide efficacy have used an outcome measure that is modeled to depend on E/I balance in the brain. In this manuscript, we present the first causal study of the effect of bumetanide on an objective marker of E/I balance in the brain, binocular rivalry, which we have previously shown to be sensitive to pharmacological manipulation of GABA. Using a within-subjects placebo-control crossover design study, we show that, contrary to expectation, acute administration of bumetanide does not alter binocular rivalry dynamics in neurotypical adult individuals. Neither changes in response times nor response criteria can account for these results. These results raise important questions about the efficacy of acute bumetanide administration for altering E/I balance in the human brain, and highlight the importance of studies using objective markers of the underlying neural processes that drugs hope to target.

neuroscience↗

An interface between spatial memory and scene perception in posterior cerebral cortex

AO_SCPLOWBSTRACTC_SCPLOWHere, we report a network of brain areas bridging the spatial-memory and scene-perception systems of the human brain. Using fine-grained individual-subject fMRI, we reveal three cortical areas of the human brain, each lying immediately anterior to a region of the scene perception network in posterior cerebral cortex, that selectively activate when recalling familiar real-world locations. Despite their close proximity to the scene-perception areas, network analyses show that these regions constitute a distinct functional network that interfaces with memory systems during naturalistic scene understanding. These "place-memory areas" offer a new framework for understanding how the brain implements memory-guided visual behaviors, including navigation.

neuroscience↗

Active Vision in Immersive, 360° Real-World Environments

Vision is an active process. Humans actively sample their sensory environment via saccades, head turns, and body movements. Yet, little is known about active visual processing in real-world environments. Here, we exploited recent advances in immersive virtual reality (VR) and in-headset eye-tracking to show that active viewing conditions impact how humans process complex, real-world scenes. Specifically, we used quantitative, model-based analyses to compare which visual features participants prioritize over others while encoding a novel environment in two experimental conditions: active and passive. In the active condition, participants used head-mounted VR displays to explore 360{o} scenes from a first-person perspective via self-directed motion (saccades and head turns). In the passive condition, 360{o} scenes were passively displayed to participants within the VR headset while they were head-restricted. Our results show that signatures of top-down attentional guidance increase in active viewing conditions: active viewers disproportionately allocate their attention to semantically relevant scene features, as compared with passive viewers. We also observed increased signatures of exploratory behavior in eye movements, such as quicker, more entropic fixations during active as compared with passive viewing conditions. These results have broad implications for studies of visual cognition, suggesting that active viewing influences every aspect of gaze behavior - from the way we move our eyes to what we choose to attend to - as we construct a sense of place in a real-world environment. Significance StatementEye-tracking in immersive virtual reality offers an unprecedented opportunity to study human gaze behavior under naturalistic viewing conditions without sacrificing experimental control. Here, we advanced this new technique to show how humans deploy attention as they encode a diverse set of 360{o}, real-world scenes, actively explored from a first-person perspective using head turns and saccades. Our results build on classic studies in psychology, showing that active, as compared with passive, viewing conditions fundamentally alter perceptual processing. Specifically, active viewing conditions increase information-seeking behavior in humans, producing faster, more entropic fixations, which are disproportionately deployed to scene areas that are rich in semantic meaning. In addition, our results offer key benchmark measurements of gaze behavior in 360{degrees}, naturalistic environments.

neuroscience↗

Adaptive shifts in gene regulation underlie a developmental delay in thermogenesis in high-altitude deer mice

Aerobic performance is tied to fitness as it influences an animals ability to find food, escape predators, or survive extreme conditions. At high altitude, where low O2 availability and persistent cold prevail, maximum metabolic heat production (thermogenesis) is an aerobic performance trait that is intimately linked to survival. Understanding how thermogenesis evolves to enhance survival at high altitude will yield insight into the links between physiology, performance, and fitness. Recent work in deer mice (Peromyscus maniculatus) has shown that adult mice native to high-altitude have higher thermogenic capacities under hypoxia compared to lowland conspecifics, but developing high-altitude pups delay the onset of thermogenesis. This suggests that natural selection on thermogenic capacity varies across life stages. To determine the mechanistic cause of this ontogenetic delay, we analyzed the transcriptomes of thermo-effector organs - brown adipose tissue and skeletal muscle - in developing deer mice native to low- and high-altitude. We demonstrate that the developmental delay in thermogenesis is associated with adaptive shifts in the expression of genes involved in nervous system development, fuel/O2 supply, and oxidative metabolism gene pathways. Our results demonstrate that selection has modified the developmental trajectory of the thermoregulatory system at high altitude and has done so by acting on the regulatory systems that control the maturation of thermo-effector tissues. We suggest that the cold and hypoxic conditions of high altitude may force a resource allocation trade-off, whereby limited energy is allocated to developmental processes such as growth, versus active thermogenesis during early development.

evolutionary biology↗