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Baker, C. I.

Publications and source records attributed to Baker, C. I..

At least 19 recordsLinked to original sources

Translating functional brain activity between humans and monkeys

Comparing brain responses across species is essential for identifying models of human cognition and testing theories of brain evolution, but differences in brain size, measurement techniques, and signal dynamics make it challenging. Here we collected dense fMRI data in macaques and humans using the same movies, static-image sequences, and tasks, and developed a multivariate analysis method that aligns neural representations temporally and spatially. The resulting data-driven framework provides a quantitative translation of brain responses among individuals and between species. Using this framework, we uncovered a broadly conserved cross-species hierarchy of retinotopic visual areas and whole-brain correspondence. Yet within this structure, we found that higher-order macaque areas shared more information with lower-order human areas, particularly during movies, providing evidence of species differences. We also identified potential macaque precursors to human regions involved in high-level cognition, including theory-of-mind and reading. These results offer a blueprint for common representational principles across species.

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Replicating the facilitatory effects of transcranial random noise stimulation on motion processing: A registered report

Non-invasive brain stimulation (NIBS) techniques have the potential to demonstrate the causal impact of targeted brain regions on specific behaviors, and to regulate or facilitate behavior in clinical applications. Transcranial random noise stimulation (tRNS) is one form of transcranial electric stimulation (tES) in which an alternating current is passed between electrodes at random frequencies. High-frequency tRNS (hf-tRNS) is thought to enhance excitability and has been reported to have facilitatory effects on behavior in healthy and clinical populations. Due to the potential application of tRNS, clear demonstrations of the efficacy and replicability of stimulation are critical. Here, we focused on replicating the facilitatory effect of hf-tRNS over the human middle temporal complex (hMT+) on contralateral motion processing, initially demonstrated by Ghin et al. (2018). In this prior study, the improvement in performance was specific to global motion processing in the visual field contralateral to stimulation. The motivation to replicate this effect was reinforced by the well-supported hypothesis that hMT+ is critical for contralateral global motion processing. However, our results indicated that hf-tRNS does not improve motion discrimination. Specifically, we were unable to replicate a contralateral global motion processing facilitation following hf-tRNS to hMT+. In our within-subject controls, we also found no difference between hf-tRNS to hMT+ on contralateral global motion processing in comparison to sham stimulation, or in comparison to hf-tRNS to the forehead. While it remains possible that our lack of replication could be due to minor changes in the protocol from the original Ghin et al., study, for hf-tRNS to become a widely applied method, the modulatory effect of hf-tRNS should be robust to slight adjustments to the procedure.

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Systematic effects of retinotopic biases and category selectivity across human occipitotemporal cortex

The organization of human visual cortex has traditionally been studied using two different methods: retinotopic mapping and category-selectivity mapping. Retinotopic mapping has identified a large number of systematic maps of the visual field, while category-selectivity mapping has identified clusters of neural populations that reliably respond more strongly to specific image categories such as objects, faces, scenes and body parts compared to other categories. While early investigations seemed to suggest that these two organizing principles were largely separated in the brain, with retinotopic maps in posterior visual cortex and category-selective regions in anterior visual cortex, recent work shows that category-selective regions overlap with retinotopic maps, giving rise to spatial visual field biases within these regions. Here, we collected fMRI responses whilst performing both retinotopic and category mapping within the same participants, allowing detailed comparison of neural tuning for space and category at the single voxel level. We use these data to evaluate two previous proposals of how retinotopic biases relate to category-selectivity: 1) complementary quadrant biases (upper vs. lower contralateral visual field) inherited from early visual cortex explain the presence of paired regions selective for the same category across lateral and ventral occipitotemporal cortex (lOTC, vOTC); and 2) eccentricity biases (center vs. periphery of the visual field) explain the presence of selectivity for different categories, specifically differentiating face-versus scene-selectivity within the ventral surface. Confirming and extending previous findings for a comprehensive set of face-, scene-, object, and place-selective regions of interest, we provide robust evidence that category-selective regions do not sample visual space uniformly, exhibiting systematic biases towards either the upper or lower field (all category regions) and center vs. periphery (face vs. place regions). Consistent with 1), we find that quadrant biases differ systematically between lateral and ventral OTC, with lateral regions showing systematic lower field biases and ventral regions showing upper field biases, differentiating regions selective for the same category in terms of their spatial bias. However, contrary to 2), we find that eccentricity tuning does not strongly predict the strength of face-or scene category-selectivity in a given voxel. Specifically, highly face-selective voxels are not solely confined to the fovea, and while most scene-selective voxels show peripheral tuning, highly scene-selective voxels actually show strong foveal tuning, particularly in anterior medial-ventral cortex. Collectively, these results demonstrate that spatial biases in category-selective cortex are widespread and robust, whilst also suggesting there is no simple relation between spatial tuning and category-selectivity.

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Graspable foods and tools elicit similar responses in visual cortex

Extrastriatal visual cortex is known to exhibit distinct response profiles to complex stimuli of varying ecological importance (e.g., faces, scenes, and tools). The dominant interpretation of these effects is that they reflect activation of distinct "category-selective" brain regions specialized to represent these and other stimulus categories. We sought to explore an alternative perspective: that the response to these stimuli is determined less by whether they form distinct categories, and more by their relevance to different forms of natural behavior. In this regard, food is an interesting test case, since it is primarily distinguished from other objects by its edibility, not its appearance, and there is evidence of food-selectivity in human visual cortex. Food is also associated with a common behavior, eating, and food consumption typically also involves the manipulation of food, often with the hands. In this context, food items share many properties in common with tools: they are graspable objects that we manipulate in self-directed and stereotyped forms of action. Thus, food items may be preferentially represented in extrastriatal visual cortex in part because of these shared affordance properties, rather than because they reflect a wholly distinct kind of category. We conducted fMRI and behavioral experiments to test this hypothesis. We found that behaviorally graspable food items and tools were judged to be similar in their action-related properties, and that the location, magnitude, and patterns of neural responses for images of graspable food items were similar in profile to the responses for tool stimuli. Our findings suggest that food-selectivity may reflect the behavioral affordances of food items rather than a distinct form of category-selectivity.

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Stable Cortical Body Maps Before and After Arm Amputation

The adult brains capacity for cortical reorganization remains debated. Using longitudinal neuroimaging in three adults, followed up to five years before and after arm amputation, we compared cortical activity elicited by movement of the hand (pre-amputation) versus phantom hand (post-amputation) and lips (pre/post-amputation). We observed stable representations of both hand and lips. By directly quantifying activity changes across amputation, we overturn decades of animal and human research, demonstrating amputation does not trigger large- scale cortical reorganization.

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Multidimensional object properties are dynamically represented in the human brain

Our visual world consists of an immense number of unique objects and yet, we are easily able to identify, distinguish, interact, and reason about the things we see within a few hundred milliseconds. This requires that we integrate and focus on a wide array of object properties to support diverse behavioral goals. In the current study, we used a large-scale and comprehensively sampled stimulus set and developed an analysis approach to determine if we could capture how rich, multidimensional object representations unfold over time in the human brain. We modelled time-resolved MEG signals evoked by viewing single presentations of tens of thousands of object images based on millions of behavioral judgments. Extracting behavior-derived object dimensions from similarity judgments, we developed a data-driven approach to guide our understanding of the neural representation of the object space and found that every dimension is reflected in the neural signal. Studying the temporal profiles for different object dimensions we found that the time courses fell into two broad types, with either a distinct and early peak ([~]125 ms) or a slow rise to a late peak ([~]300 ms). Further, early effects were stable across participants, in contrast to later effects which showed more variability, suggesting that early peaks may carry stimulus-specific and later peaks more participant-specific information. Dimensions with early peaks appeared to be primarily visual dimensions and those with later peaks more conceptual, suggesting that conceptual representations are more variable across people. Together, these data provide a comprehensive account of how behavior-derived object properties unfold in the human brain and form the basis for the rich nature of object vision.

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Distributed representations of behaviorally relevant object dimensions in the human visual system

Object vision is commonly thought to involve a hierarchy of brain regions processing increasingly complex image features, with high-level visual cortex supporting object recognition and categorization. However, object vision supports diverse behavioral goals, suggesting basic limitations of this category-centric framework. To address these limitations, we mapped a series of dimensions derived from a large-scale analysis of human similarity judgments directly onto the brain. Our results reveal broadly distributed representations of behaviorally-relevant information, demonstrating selectivity to a wide variety of novel dimensions while capturing known selectivities for visual features and categories. Behavior-derived dimensions were superior to categories at predicting brain responses, yielding mixed selectivity in much of visual cortex and sparse selectivity in category-selective clusters. This framework reconciles seemingly disparate findings regarding regional specialization, explaining category selectivity as a special case of sparse response profiles among representational dimensions, suggesting a more expansive view on visual processing in the human brain.

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Should bionic limb control mimic the human body? Impact of control strategy on bionic hand skill learning

A longstanding engineering ambition has been to design anthropomorphic bionic limbs: devices that look like and are controlled in the same way as the biological body (biomimetic). The untested assumption is that biomimetic motor control enhances device embodiment, learning, generalization, and automaticity. To test this, we compared biomimetic and non-biomimetic control strategies for able-bodied participants when learning to operate a wearable myoelectric bionic hand. We compared motor learning across days and behavioural tasks for two training groups: Biomimetic (mimicking the desired bionic hand gesture with biological hand) and Arbitrary control (mapping an unrelated biological hand gesture with the desired bionic gesture). For both trained groups, training improved bionic limb control, reduced cognitive reliance, and increased embodiment over the bionic hand. Biomimetic users had more intuitive and faster control early in training. Arbitrary users matched biomimetic performance later in training. Further, arbitrary users showed increased generalization to a novel control strategy. Collectively, our findings suggest that biomimetic and arbitrary control strategies provide different benefits. The optimal strategy is likely not strictly biomimetic, but rather a flexible strategy within the biomimetic to arbitrary spectrum, depending on the user, available training opportunities and user requirements.

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Distributed cortical regions for the recall of people, places and objects

Human medial parietal cortex (MPC) is recruited during multiple cognitive processes. Previously, we demonstrated regions specific to recall of people or places and proposed that the functional organization of MPC mirrors the category selectivity defining the medial-lateral axis of ventral temporal cortex (VTC). However, prior work considered recall of people and places only and VTC also shows object-selectivity sandwiched between face- and scene-selective regions. Here, we tested a strong prediction of our proposal: like VTC, MPC should show a region specifically recruited during object recall, and its relative cortical position should mirror the one of VTC. While responses during people and place recall showed a striking replication of prior findings, we did not observe any evidence for object-recall effects within MPC, which differentiates it from the spatial organization in VTC. Importantly, beyond MPC, robust recall-effects were observed for people, places, and objects on the lateral surface of the brain. Place-recall effects were present in the angular gyrus, frontal eye fields and peripheral portions of early visual cortex, whereas people-recall selectively drove response in the right posterior superior temporal sulcus. Object-recall effects were largely restricted to a region posterior to left somatosensory cortex, in the vicinity of the supramarginal gyrus. Taken together, these data demonstrate that while there are distributed regions active during recall of people, places and objects, the functional organization of MPC does not mirror the medial-lateral axis of VTC but reflects only the most salient features of that axis - namely representations of people and places. Significance statementHuman medial parietal cortex (MPC) is recruited during multiple cognitive processes. Recently, we proposed a framework for interpreting the functional organization of MPC by suggesting that it reflects the categorical preferences for people and places that is evident also in ventral temporal cortex (VTC). Because VTC also exhibits selectivity for objects, we here extend this framework to test whether MPC also shows object selectivity during recall. Robust people and place recall effects were evident in MPC, but we found no evidence for object-recall within MPC, suggesting that MPC and VTC are not mirror-copies of each other. Together, these data suggest that the functional organization of MPC reflects the most salient categorical representations within VTC for people and places.

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Multidimensional topography of memory revealed from thousands of daily documented memories

Our memories form a rich, colorful tapestry of emotions, events, people, and places, woven across the decades of our lives. However, research has typically been limited in its ability to assess the multidimensional nature of episodic memory, given the short time scales and artificial stimulus sets often required in experiments. In an era when people are constantly recording their lives through social media, we can now examine key questions about the behavioral and neural underpinnings of diverse and extensive real-world memories. Here, we tested the neural representations of episodic memory in a naturalistic setting, specifically focusing on the age, location, subjective memory strength, and emotional content of memories. We recruited 23 users of a video diary app ("1 Second Everyday"), who had recorded a total of 9,266 daily memory videos spanning up to 7 years prior to our study. During a 3T fMRI scan, participants viewed a set of 300 of their own memory videos intermixed with 300 videos from another individual. We identified key areas specifically engaged for ones own memories versus anothers. Delving into the multidimensional nature of these memories, we find that their features are tightly interrelated, highlighting the need to consider these features in conjunction when conducting memory research. Importantly, when looking at the distinct contributions of these features, we find a topography of memory content extending across the medial parietal lobe with separate representations of a memorys age, its strength, and the familiarity of the people and places involved.

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THINGS-data: A multimodal collection of large-scale datasets for investigating object representations in brain and behavior

Understanding object representations requires a broad, comprehensive sampling of the objects in our visual world with dense measurements of brain activity and behavior. Here we present THINGS-data, a multimodal collection of large-scale neuroimaging and behavioral datasets in humans, comprising densely-sampled functional MRI and magnetoencephalographic recordings, as well as 4.70 million similarity judgments in response to thousands of photographic images for up to 1,854 object concepts. THINGS-data is unique in its breadth of richly-annotated objects, allowing for testing countless hypotheses at scale while assessing the reproducibility of previous findings. Beyond the unique insights promised by each individual dataset, the multimodality of THINGS-data allows combining datasets for a much broader view into object processing than previously possible. Our analyses demonstrate the high quality of the datasets and provide five examples of hypothesis-driven and data-driven applications. THINGS-data constitutes the core public release of the THINGS initiative (https://things-initiative.org) for bridging the gap between disciplines and the advancement of cognitive neuroscience.

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The Features Underlying the Memorability of Objects

What makes certain images more memorable than others? While much of memory research has focused on participant effects, recent studies employing a stimulus-centric perspective have sparked debate on the determinants of memory, including the roles of semantic and visual features and whether the most prototypical or atypical items are best remembered. Prior studies have typically relied on constrained stimulus sets, limiting a generalized view of the features underlying what we remember. Here, we collected 1+ million memory ratings for a naturalistic dataset of 26,107 object images designed to comprehensively sample concrete objects. We establish a model of object features that is predictive of image memorability and examined whether memorability could be accounted for by the typicality of the objects. We find that semantic features exert a stronger influence than perceptual features on what we remember and that the relationship between memorability and typicality is more complex than a simple positive or negative association alone. TEASERSemantic versus perceptual features more heavily influence what we remember, and memorability cannot be reduced to typicality.

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An empirically-driven guide on using Bayes Factors for M/EEG decoding

Bayes Factors can be used to provide quantifiable evidence for contrasting hypotheses and have thus become increasingly popular in cognitive science. However, Bayes Factors are rarely used to statistically assess the results of neuroimaging experiments. Here, we provide an empirically-driven guide on implementing Bayes Factors for time-series neural decoding results. Using real and simulated Magnetoencephalography (MEG) data, we examine how parameters such as the shape of the prior and data size affect Bayes Factors. Additionally, we discuss benefits Bayes Factors bring to analysing multivariate pattern analysis data and show how using Bayes Factors can be used instead or in addition to traditional frequentist approaches.

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Direct comparison of category and spatial selectivity in human occipitotemporal cortex

Human visual cortex is organised broadly according to two major principles: retinotopy (the spatial mapping of the retina in cortex) and category-selectivity (preferential responses to specific categories of stimuli). Historically, these principles were considered anatomically separate, with retinotopy restricted to the occipital cortex and category-selectivity emerging in the lateral-occipital and ventral-temporal cortex. However, recent studies show that category-selective regions exhibit systematic retinotopic biases, for example exhibiting stronger activation for stimuli presented in the contra- compared to the ipsilateral visual field. It is unclear, however, whether responses within category-selective regions are more strongly driven by retinotopic location or by category preference, and if there are systematic differences between category-selective regions in the relative strengths of these preferences. Here, we directly compare contralateral and category preferences by measuring fMRI responses to scene and face stimuli presented in the left or right visual field and computing two bias indices: a contralateral bias (response to the contralateral minus ipsilateral visual field) and a face/scene bias (preferred response to scenes compared to faces, or vice versa). We compare these biases within and between scene- and face-selective regions and across the lateral and ventral surfaces of visual cortex more broadly. We find an interaction between surface and bias: lateral surface regions show a stronger contralateral than face/scene bias, whilst ventral surface regions show the opposite. These effects are robust across and within subjects, and appear to reflect large-scale, smoothly varying gradients. Together, these findings support distinct functional roles for lateral and ventral visual cortex in terms of the relative importance of the spatial location of stimuli during visual information processing.

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Multiple adjoining word and face selective regions in ventral temporal cortex exhibit distinct dynamics

The map of category-selectivity in human ventral temporal cortex (VTC) provides organizational constraints to models of object recognition. One important principle is lateral-medial response biases to stimuli that are typically viewed in the center or periphery of the visual field. However, little is known about the relative temporal dynamics and location of regions that respond preferentially to stimulus classes that are centrally viewed, like the face- and word-processing networks. Here, word- and face-selective regions within VTC were mapped using intracranial recordings from 36 patients. Partially overlapping, but also anatomically dissociable patches of face- and word-selectivity were found in VTC. In addition to canonical word-selective regions along the left posterior occipitotemporal sulcus, selectivity was also located medial and anterior to face-selective regions on the fusiform gyrus at the group level and within individual subjects. These regions were replicated using 7 Tesla fMRI in healthy subjects. Left hemisphere word-selective regions preceded right hemisphere responses by 125 ms, potentially reflecting the left hemisphere bias for language; with no hemispheric difference in face-selective response latency. Word-selective regions along the posterior fusiform responded first, then spread medially and laterally, then anteriorally. Face-selective responses were first seen in posterior fusiform regions bilaterally, then proceeded anteriorally from there. For both words and faces, the relative delay between regions was longer than would be predicted by purely feedforward models of visual processing. The distinct time-courses of responses across these regions, and between hemispheres, suggest a complex and dynamic functional circuit supports face and word perception. Significance StatementRepresentations of visual objects in the human brain have been shown to be organized by several principles, including whether those objects tend to be viewed centrally or peripherally in the visual field. However, it remains unclear how regions that process objects that are viewed centrally, like words and faces, are organized relative to one another. Here, invasive and non-invasive neuroimaging suggests there is a mosaic of regions in ventral temporal cortex that respond selectively to either words or faces. These regions display differences in the strength and timing of their responses, both within and between brain hemispheres, suggesting they play different roles in perception. These results illuminate extended, bilateral, and dynamic brain pathways that support face perception and reading.

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TMS of lateral occipital cortex reduces BOLD responses across category-selective areas in ventral temporal cortex

Human visual cortex contains three scene-selective regions in the lateral, medial and ventral cortex, termed the occipital place area (OPA), medial place area (MPA) and parahippocampal place area (PPA). Using functional magnetic resonance imaging (fMRI), all three regions respond more strongly when viewing visual scenes compared with isolated objects or faces. To determine how these regions are functionally and causally connected, we applied transcranial magnetic stimulation to OPA and measured fMRI responses before and after stimulation, using a theta-burst paradigm (TBS). To test for stimulus category-selectivity, we presented a range of visual categories (scenes, buildings, objects, faces). To test for specificity of any effects to TBS of OPA we employed two control conditions: Sham, with no TBS stimulation, and an active TBS-control with TBS to a proximal face-selective cortical region (occipital face area, or OFA). We predicted that TBS to OPA (but not OFA) would lead to decreased responses to scenes and buildings (but not other categories) in other scene-selective cortical regions. Across both ROI and whole-volume analyses, we observed decreased responses to scenes in PPA as a result of TBS. However, these effects were neither category specific, with decreased responses to all stimulus categories, nor limited to scene-selective regions, with decreases also observed in face-selective fusiform face area (FFA). Furthermore, similar effects were observed with TBS to OFA, thus effects were not specific to the stimulation site in the lateral occipital cortex. Whilst these data are suggestive of a causal, but non-specific relationship between lateral occipital and ventral temporal cortex, we discuss several factors that could have underpinned this result, such as the differences between TBS and online TMS, the role of anatomical distance between stimulated regions and how TMS effects are operationalised. Furthermore, our findings highlight the importance of active control conditions in brain stimulation experiments to accurately assess functional and causal connectivity between specific brain regions.

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Representation of contralateral visual space in the human hippocampus

The initial encoding of visual information primarily from the contralateral visual field is a fundamental organizing principle of the primate visual system. Recently, the presence of such retinotopic sensitivity has been shown to extend well beyond early visual cortex to regions not historically considered retinotopically sensitive. In particular, human scene-selective regions in parahippocampal and medial parietal cortex exhibit prominent biases for the contralateral visual field. Here we used fMRI to test the hypothesis that the human hippocampus, which is thought to be anatomically connected with these scene-selective regions, would also exhibit a biased representation of contralateral visual space. First, population receptive field mapping with scene stimuli revealed strong biases for the contralateral visual field in bilateral hippocampus. Second, the distribution of retinotopic sensitivity suggested a more prominent representation in anterior medial portions of the hippocampus. Finally, the contralateral bias was confirmed in independent data taken from the Human Connectome Project initiative. The presence of contralateral biases in the hippocampus - a structure considered by many as the apex of the visual hierarchy - highlights the truly pervasive influence of retinotopy. Moreover, this finding has important implications for understanding how this information relates to the allocentric global spatial representations known to be encoded therein. Significance StatementRetinotopic encoding of visual information is an organizing principle of visual cortex. Recent work demonstrates this sensitivity in structures far beyond early visual cortex, including those anatomically connected to the hippocampus. Here, using population receptive field modelling in two independent sets of data we demonstrate a consistent bias for the contralateral visual field in bilateral hippocampus. Such a bias highlights the truly pervasive influence of retinotopy, with important implications for understanding how the presence of retinotopy relates to more allocentric spatial representations.

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Disrupted object-scene semantics boost scene recall but diminish object recall in drawings from memory

Humans are highly sensitive to the statistical relationships between features and objects within visual scenes. Inconsistent objects within scenes (e.g., a mailbox in a bedroom) instantly jump out to us, and are known to capture our attention. However, it is debated whether such semantic inconsistencies result in boosted memory for the scene, impaired memory, or have no influence on memory. Here, we examined the relationship of scene-object consistencies on memory representations measured through drawings made during recall. Participants (N=30) were eye-tracked while studying 12 real-world scene images with an added object that was either semantically consistent or inconsistent. After a 6-minute distractor task, they drew the scenes from memory while pen movements were tracked electronically. Online scorers (N=1,725) rated each drawing for diagnosticity, object detail, spatial detail, and memory errors. Inconsistent scenes were recalled more frequently, but contained less object detail. Further, inconsistent objects elicited more errors reflecting looser memory binding (e.g., migration across images). These results point to a dual effect in memory of boosted global (scene) but diminished local (object) information. Finally, we replicated prior effects showing that inconsistent objects captured eye fixations, but found that fixations during study were not correlated with recall performance, time, or drawing order. In sum, these results show a nuanced effect of scene inconsistencies on memory detail during recall.

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