Dataset Information

Predicting the Multisensory Consequences of One's Own Action: BOLD Suppression in Auditory and Visual Cortices.

ABSTRACT: Predictive mechanisms are essential to successfully interact with the environment and to compensate for delays in the transmission of neural signals. However, whether and how we predict multisensory action outcomes remains largely unknown. Here we investigated the existence of multisensory predictive mechanisms in a context where actions have outcomes in different modalities. During fMRI data acquisition auditory, visual and auditory-visual stimuli were presented in active and passive conditions. In the active condition, a self-initiated button press elicited the stimuli with variable short delays (0-417ms) between action and outcome, and participants had to detect the presence of a delay for auditory or visual outcome (task modality). In the passive condition, stimuli appeared automatically, and participants had to detect the number of stimulus modalities (unimodal/bimodal). For action consequences compared to identical but unpredictable control stimuli we observed suppression of the blood oxygen level depended (BOLD) response in a broad network including bilateral auditory and visual cortices. This effect was independent of task modality or stimulus modality and strongest for trials where no delay was detected (undetected

SUBMITTER: Straube B

PROVIDER: S-EPMC5218407 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Predicting the Multisensory Consequences of One's Own Action: BOLD Suppression in Auditory and Visual Cortices.

Straube Benjamin B van Kemenade Bianca M BM Arikan B Ezgi BE Fiehler Katja K Leube Dirk T DT Harris Laurence R LR Kircher Tilo T

PloS one 20170106 1

Predictive mechanisms are essential to successfully interact with the environment and to compensate for delays in the transmission of neural signals. However, whether and how we predict multisensory action outcomes remains largely unknown. Here we investigated the existence of multisensory predictive mechanisms in a context where actions have outcomes in different modalities. During fMRI data acquisition auditory, visual and auditory-visual stimuli were presented in active and passive conditions ...[more]

PMID: 28060861

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Project description:When the brain tries to acquire an elaborate model of the world, multisensory integration should contribute to building predictions based on the various pieces of information, and deviance detection should repeatedly update these predictions by detecting "errors" from the actual sensory inputs. Accumulating evidence such as a hierarchical organization of the deviance-detection system indicates that the deviance-detection system can be interpreted in the predictive coding framework. Herein, we targeted mismatch negativity (MMN) as a type of prediction-error signal and investigated the relationship between multisensory integration and MMN. In particular, we studied whether and how cross-modal information processing affected MMN in rodents. We designed a new surface microelectrode array and simultaneously recorded visual and auditory evoked potentials from the visual and auditory cortices of rats under anesthesia. Then, we mapped MMNs for five types of deviant stimuli: single-modal deviants in (i) the visual oddball and (ii) auditory oddball paradigms, eliciting single-modal MMN; (iii) congruent audio-visual deviants, (iv) incongruent visual deviants, and (v) incongruent auditory deviants in the audio-visual oddball paradigm, eliciting cross-modal MMN. First, we demonstrated that visual MMN exhibited deviance detection properties and that the first-generation focus of visual MMN was localized in the visual cortex, as previously reported in human studies. Second, a comparison of MMN amplitudes revealed a non-linear relationship between single-modal and cross-modal MMNs. Moreover, congruent audio-visual MMN exhibited characteristics of both visual and auditory MMNs-its latency was similar to that of auditory MMN, whereas local blockage of N-methyl-D-aspartic acid receptors in the visual cortex diminished it as well as visual MMN. These results indicate that cross-modal information processing affects MMN without involving strong top-down effects, such as those of prior knowledge and attention. The present study is the first electrophysiological evidence of cross-modal MMN in animal models, and future studies on the neural mechanisms combining multisensory integration and deviance detection are expected to provide electrophysiological evidence to confirm the links between MMN and predictive coding theory.

Project description:Orientation processing in the human brain plays a crucial role in guiding grasping actions toward an object. Remarkably, despite the absence of visual input, the human visual cortex can still process orientation information. Instead of visual input, non-visual information, including tactile and proprioceptive sensory input from the hand and arm, as well as feedback from action-related processes, may contribute to orientation processing. However, the precise mechanisms by which the visual cortices process orientation information in the context of non-visual sensory input and action-related processes remain to be elucidated. Thus, our study examined the orientation representation within the visual cortices by analyzing the blood-oxygenation-level-dependent (BOLD) signals under four action conditions: direct grasp (DG), air grasp (AG), non-grasp (NG), and uninformed grasp (UG). The images of the cylindrical object were shown at +45° or - 45° orientations, corresponding to those of the real object to be grasped with the whole-hand gesture. Participants judged their orientation under all conditions. Grasping was performed without online visual feedback of the hand and object. The purpose of this design was to investigate the visual areas under conditions involving tactile feedback, proprioception, and action-related processes. To address this, a multivariate pattern analysis was used to examine the differences among the cortical patterns of the four action conditions in orientation representation by classification. Overall, significant decoding accuracy over chance level was discovered for the DG; however, during AG, only the early visual areas showed significant accuracy, suggesting that the object's tactile feedback influences the orientation process in higher visual areas. The NG showed no statistical significance in any area, indicating that without the grasping action, visual input does not contribute to cortical pattern representation. Interestingly, only the dorsal and ventral divisions of the third visual area (V3d and V3v) showed significant decoding accuracy during the UG despite the absence of visual instructions, suggesting that the orientation representation was derived from action-related processes in V3d and visual recognition of object visualization in V3v. The processing of orientation information during non-visually guided grasping of objects relies on other non-visual sources and is specifically divided by the purpose of action or recognition.

Dataset Information

Predicting the Multisensory Consequences of One's Own Action: BOLD Suppression in Auditory and Visual Cortices.

Publications

Predicting the Multisensory Consequences of One's Own Action: BOLD Suppression in Auditory and Visual Cortices.

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