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Steel, A.

Publications and source records attributed to Steel, A..

14 recordsLinked to original sources

Multiple forms of sensory reinstatement in category-selective cortex

Visual recall is classically thought to depend on reinstatement: areas engaged when encoding a visual input are similarly reactivated when remembering it. Here we investigated if reinstatement might be differently implemented across the diverse category-selective systems of visual cortex. Using fMRI in 25 participants, we assessed possible reinstatement organizations across scene-, face-, and body-selective cortex. We asked whether memory reactivates the same category-selective areas engaged during perception, whether it engages same or distinct vertices, and whether perceptual-mnemonic distinctions were topographically organized. All regions were selectively engaged during both perception and memory, though memory activity was weaker overall. At the vertex-level, most regions--including body-selective LOS, ITG, MTG; face-selective FFA1, FFA2; and scene-selective PPA--showed classic reinstatement, with memory enriched in the most perceptually selective vertices. In contrast, OFA and OPA showed separable perception-and memory-biased vertices. Critically, only scene-selective areas showed topographic distinction: in both PPA and OPA, mnemonic activity was located consistently anterior to perceptual activity, whereas no face-or body-selective areas showed such a distinction. Thus, while all category-selective areas are reactivated during memory, scene-selective cortex topographically separates memory from perception, suggesting different sensory reinstatement implementations across high-level visual cortex, possibly reflecting the distinct computational demands.

neuroscience↗

Scene perception-memory pairing extends to superior parietal cortex

Visual scene analysis relies on a set of scene-selective regions in posterior cerebral cortex (OPA, PPA, MPA), with a paired memory-responsive counterpart located in anterior (LPMA, VPMA) or overlapping cortex (MPMA). The interaction between these pairs of regions is thought to integrate visual input with mnemonic context. Recently, a fourth scene-perception area in superior parietal cortex (SPA) was identified, with a proposed role in visually-guided navigation. Whether this region also has an anterior paired memory region is currently unknown. Across two independent fMRI datasets (total N=24, 14 females) using static or dynamic stimuli and distinct memory tasks, we show that recalling visual scenes evokes robust responses in a region (referred to here as SPMA) immediately anterior and dorsal to SPA. During resting-state fMRI, SPA preferentially coupled with the other scene-perception areas, while SPMA preferentially coupled with the other place memory areas. At the whole-brain level, seed-based connectivity revealed that SPA sits at the confluence of four processing streams spanning regions implicated in egocentric scene perception, map-based navigation, perspective taking, and goal-directed movement. These findings extend the perception-memory motif associated with visual scene processing to the fourth cortical surface. The widespread anatomical coupling between scene-perception and memory processes reflects the importance of this interaction for flexible, context-grounded navigation.

neuroscience↗

DNA methylation reprogramming in marsupial embryos is restricted to the extraembryonic lineage

DNA methylation (5mC) is an epigenetic mark that plays a critical role in defining cell fate. Following fertilisation, DNA methylation inherited from gametes must be reprogrammed to establish totipotency and enable the parental-to-zygotic transition. To accomplish this, non-mammalian vertebrates such as zebrafish and medaka subtly reprogram maternal 5mC profiles while maintaining high methylation levels throughout embryogenesis. In contrast, eutherian mammals such as mouse and human undergo global 5mC erasure in both embryonic and extraembryonic lineages. However, while embryonic 5mC is rapidly re-established to high levels upon implantation, the trophectoderm, which gives rise to the placenta, displays sustained and conserved DNA hypomethylation, suggesting that this drastic 5mC erasure may be functionally linked to complex placentation in mammals. To clarify whether extensive post-fertilisation 5mC erasure co-evolved with placentation, we explored embryonic methylation dynamics in marsupials, a lineage of therian mammals with a short-lived placenta. We produced a near complete telomere-to-telomere (T2T) genome and generated detailed epigenome maps of embryonic development for an Australian marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). We found the dunnart embryo exhibits genome wide DNA demethylation at the blastocyst stage, but these changes occur in the trophectoderm only, suggesting that 5mC erasure in the placenta is an ancestral state in therian mammals. Furthermore, the T2T-level dunnart genome assembly enabled identification of sex chromosomes, uncovering extensive hypomethylation of the paternally-inherited inactive X chromosome in females and revealing the previously unannotated master regulator of X chromosome inactivation, lncRNA Rsx. Our data indicate that while the use of genome-wide 5mC erasure differs between eutherian and marsupial lineages, 5mC erasure in extraembryonic tissue is ancestral to therian mammals and may be necessary to support placental development. HIGHLIGHTSO_LIFirst embryonic DNA methylation maps in an Australian marsupial C_LIO_LIExtensive global erasure of DNA methylation in the trophectoderm C_LIO_LIMaintenance of high DNA methylation in the embryonic lineage C_LIO_LIHypomethylated paternal X chromosome with methylated escapee genes C_LI

developmental biology↗

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↗

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↗

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↗

Intention to learn modulates the impact of reward and punishment on sequence learning

In real-world settings, learning is often characterised as intentional: learners are aware of the goal during the learning process, and the goal of learning is readily dissociable from the awareness of what is learned. Recent evidence has shown that reward and punishment (collectively referred to as valenced feedback) are important factors that influence performance during learning. Presently, however, studies investigating the impact of valenced feedback on skill learning have only considered unintentional learning, and therefore the interaction between intentionality and valenced feedback has not been systematically examined. The present study investigated how reward and punishment impact behavioural performance when participants are instructed to learn in a goal-directed fashion (i.e. intentionally) rather than unintentionally. In Experiment 1, participants performed the serial response time task with reward, punishment, or control feedback and were instructed to ignore the presence of the sequence, i.e., learn unintentionally. Experiment 2 followed the same design, but participants were instructed to intentionally learn the sequence. We found that punishment was significantly beneficial to performance during learning only when participants learned unintentionally, and we observed no effect of punishment when participants learned intentionally. Thus, the impact of feedback on performance may be influenced by goal of the learner.

neuroscience↗

Distinct subdivisions of human medial parietal cortex are recruited differentially for memory recall of places and people

Human medial parietal cortex (MPC) is implicated in multiple cognitive processes including memory recall, visual scene processing and navigation. It is also considered a core component of the default mode network. Here, we combine fMRI data across three independent experiments to demonstrate distinct subdivisions of MPC that are selectively recruited during memory recall of either specific places or specific people. First, distinct regions of MPC were identified on the basis of differential functional connectivity with medial and lateral regions of anterior ventral temporal cortex (VTC). Second, these same medial regions exhibited differential responses to the visual presentation of different stimulus categories, with clear preferences for scenes and faces, respectively. Third, and most critically, these regions were selectively recruited during either place or people memory recall. These subdivisions also showed a striking relationship with ventral and dorsal divisions of the default mode network. Taken together, these data reveal distinct subdivisions within MPC for the recall of places and people and moreover, suggest that the organizing principle defining the medial-lateral axis of VTC is reflected in MPC, but in the context of memory recall.

neuroscience↗

Similarity judgments and cortical visual responses reflect different properties of object and scene categories in naturalistic images

Numerous factors have been reported to underlie the representation of complex images in high-level human visual cortex, including categories (e.g. faces, objects, scenes), animacy, and real-world size, but the extent to which this organization is reflected in behavioral judgments of real-world stimuli is unclear. Here, we compared representations derived from explicit similarity judgments and ultra-high field (7T) fMRI of human visual cortex for multiple exemplars of a diverse set of naturalistic images from 48 object and scene categories. Behavioral judgements revealed a coarse division between man-made (including humans) and natural (including animals) images, with clear groupings of conceptually-related categories (e.g. transportation, animals), while these conceptual groupings were largely absent in the fMRI representations. Instead, fMRI responses tended to reflect a separation of both human and non-human faces/bodies from all other categories. This pattern yielded a statistically significant, but surprisingly limited correlation between the two representational spaces. Further, comparison of the behavioral and fMRI representational spaces with those derived from the layers of a deep neural network (DNN) showed a strong correspondence with behavior in the top-most layer and with fMRI in the mid-level layers. These results suggest that there is no simple mapping between responses in high-level visual cortex and behavior - each domain reflects different visual properties of the images and responses in high-level visual cortex may correspond to intermediate stages of processing between basic visual features and the conceptual categories that dominate the behavioral response.\n\nSignificance StatementIt is commonly assumed there is a correspondence between behavioral judgments of complex visual stimuli and the response of high-level visual cortex. We directly compared these representations across a diverse set of naturalistic object and scene categories and found a surprisingly and strikingly different representational structure. Further, both types of representation showed good correspondence with a deep neural network, but each correlated most strongly with different layers. These results show that behavioral judgments reflect more conceptual properties and visual cortical fMRI responses capture more general visual features. Collectively, our findings highlight that great care must be taken in mapping the response of visual cortex onto behavior, which clearly reflect different information.

neuroscience↗

Reward and punishment differentially recruit cerebellum and medial temporal lobe to facilitate skill memory retention

Reward and punishment shape behavior, but the mechanisms underlying their effect on skill learning are not well understood. Here, we tested whether the functional connectivity of premotor cortex (PMC), a region known to be critical for learning of sequencing skills, is altered after training by reward or punishment given during training. Resting-state fMRI was collected in two experiments before and after participants trained on either a serial reaction time task (SRTT; n = 36) or force-tracking task (FTT; n = 36) with reward, punishment, or control feedback. In each experiment, training-related change in PMC functional connectivity was compared across feedback groups. In both tasks, reward and punishment differentially affected PMC functional connectivity. On the SRTT, participants trained with reward showed an increase in functional connectivity between PMC and cerebellum as well as PMC and striatum, while participants trained with punishment showed an increase in functional connectivity between PMC and medial temporal lobe connectivity. After training on the FTT, subjects trained with control and reward showed increases in PMC connectivity with parietal and temporal cortices after training, while subjects trained with punishment showed increased PMC connectivity with ventral striatum. While the results from the two experiments overlapped in some areas, including ventral pallidum, temporal lobe, and cerebellum, these regions showed diverging patterns of results across the two tasks for the different feedback conditions. These findings suggest that reward and punishment strongly influence spontaneous brain activity after training, and that the regions implicated depend on the task learned.

neuroscience↗