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Neural activity underlying the detection of an object movement by an observer during forward self-motion: Dynamic decoding and temporal evolution of directional cortical connectivity.

ABSTRACT: Relatively little is known about how the human brain identifies movement of objects while the observer is also moving in the environment. This is, ecologically, one of the most fundamental motion processing problems, critical for survival. To study this problem, we used a task which involved nine textured spheres moving in depth, eight simulating the observer's forward motion while the ninth, the target, moved independently with a different speed towards or away from the observer. Capitalizing on the high temporal resolution of magnetoencephalography (MEG) we trained a Support Vector Classifier (SVC) using the sensor-level data to identify correct and incorrect responses. Using the same MEG data, we addressed the dynamics of cortical processes involved in the detection of the independently moving object and investigated whether we could obtain confirmatory evidence for the brain activity patterns used by the classifier. Our findings indicate that response correctness could be reliably predicted by the SVC, with the highest accuracy during the blank period after motion and preceding the response. The spatial distribution of the areas critical for the correct prediction was similar but not exclusive to areas underlying the evoked activity. Importantly, SVC identified frontal areas otherwise not detected with evoked activity that seem to be important for the successful performance in the task. Dynamic connectivity further supported the involvement of frontal and occipital-temporal areas during the task periods. This is the first study to dynamically map cortical areas using a fully data-driven approach in order to investigate the neural mechanisms involved in the detection of moving objects during observer's self-motion.

SUBMITTER: Kozhemiako N

PROVIDER: S-EPMC7680311 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The task of parceling perceived visual motion into self- and object motion components is critical to safe and accurate visually guided navigation. In this paper, we used functional magnetic resonance imaging to determine the cortical areas functionally active in this task and the pattern connectivity among them to investigate the cortical regions of interest and networks that allow subjects to detect object motion separately from induced self-motion. Subjects were presented with nine textured objects during simulated forward self-motion and were asked to identify the target object, which had an additional, independent motion component toward or away from the observer. Cortical activation was distributed among occipital, intra-parietal and fronto-parietal areas. We performed a network analysis of connectivity data derived from partial correlation and multivariate Granger causality analyses among functionally active areas. This revealed four coarsely separated network clusters: bilateral V1 and V2; visually responsive occipito-temporal areas, including bilateral LO, V3A, KO (V3B) and hMT; bilateral VIP, DIPSM and right precuneus; and a cluster of higher, primarily left hemispheric regions, including the central sulcus, post-, pre- and sub-central sulci, pre-central gyrus, and FEF. We suggest that the visually responsive networks are involved in forming the representation of the visual stimulus, while the higher, left hemisphere cluster is involved in mediating the interpretation of the stimulus for action. Our main focus was on the relationships of activations during our task among the visually responsive areas. To determine the properties of the mechanism corresponding to the visual processing networks, we compared subjects' psychophysical performance to a model of object motion detection based solely on relative motion among objects and found that it was inconsistent with observer performance. Our results support the use of scene context (e.g., eccentricity, depth) in the detection of object motion. We suggest that the cortical activation and visually responsive networks provide a potential substrate for this computation.

Project description:Movement preparation and initiation have been shown to involve large scale brain networks. Recent findings suggest that movement preparation and initiation are represented in functionally distinct cortical networks. In electroencephalographic (EEG) recordings, movement initiation is reflected as a strong negative potential at medial central channels that is phase-locked to the movement onset - the movement-related cortical potential (MRCP). Movement preparation describes the process of transforming high level movement goals to low level commands. An integral part of this transformation process is directional processing (i.e., where to move). The processing of movement direction during visuomotor and oculomotor tasks is associated with medial parieto-occipital cortex (PO) activity, phase-locked to the presentation of potential movement goals. We surmised that the network generating the MRCP (movement initiation) would encode less information about movement direction than the parieto-occipital network processing movement direction. Here, we studied delta band EEG activity during center-out reaching movements (2D; 4 directions) in visuomotor and oculomotor tasks. In 15 healthy participants, we found a consistent representation of movement direction in PO 300-400 ms after the direction cue irrespective of the task. Despite generating the MRCP, sensorimotor areas (SM) encoded less information about the movement direction than PO. Moreover, the encoded directional information in SM was less consistent across participants and specific to the visuomotor task. In a classification approach, we could infer the four movement directions from the delta band EEG activity with moderate accuracies up to 55.9%. The accuracies for cue-aligned data were significantly higher than for movement onset-aligned data in either task, which also suggests a stronger representation of movement direction during movement preparation. Therefore, we present direct evidence that EEG delta band amplitude modulations carry information about both arm movement initiation and movement direction, and that they are represented in two distinct cortical networks.

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Neural activity underlying the detection of an object movement by an observer during forward self-motion: Dynamic decoding and temporal evolution of directional cortical connectivity.

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