Different contributions of efferent and reafferent feedback to sensorimotor temporal recalibration
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ABSTRACT:
SUBMITTER: Arikan B
PROVIDER: S-EPMC8604902 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The capacity to rapidly adjust perceptual representations confers a fundamental advantage when confronted with a constantly changing world. Unexplored is how feedback regarding sensory judgments (top-down factors) interacts with sensory statistics (bottom-up factors) to drive long- and short-term recalibration of multisensory perceptual representations. Here, we examined the time course of both cumulative and rapid temporal perceptual recalibration for individuals completing an audiovisual simultaneity judgment task in which they were provided with varying degrees of feedback. We find that in the presence of feedback (as opposed to simple sensory exposure) temporal recalibration is more robust. Additionally, differential time courses are seen for cumulative and rapid recalibration dependent upon the nature of the feedback provided. Whereas cumulative recalibration effects relied more heavily on feedback that informs (i.e., negative feedback) rather than confirms (i.e., positive feedback) the judgment, rapid recalibration shows the opposite tendency. Furthermore, differential effects on rapid and cumulative recalibration were seen when the reliability of feedback was altered. Collectively, our findings illustrate that feedback signals promote and sustain audiovisual recalibration over the course of cumulative learning and enhance rapid trial-to-trial learning. Furthermore, given the differential effects seen for cumulative and rapid recalibration, these processes may function via distinct mechanisms.
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Project description:The characteristic temporal relationship between actions and their sensory outcomes allows us to distinguish self- from externally generated sensory events. However, the complex sensory environment can cause transient delays between action and outcome calling for flexible recalibration of predicted sensorimotor timing. Since the neural underpinnings of this process are largely unknown this study investigated the involvement of the cerebellum by means of cerebellar transcranial direct current stimulation (ctDCS). While receiving anodal, cathodal, dual-hemisphere or sham ctDCS, in an adaptation phase, participants were exposed to constant delays of 150 ms between actively or passively generated button presses and visual sensory outcomes. Recalibration in the same (visual outcome) and in another sensory modality (auditory outcome) was assessed in a subsequent test phase during which variable delays between button press and visual or auditory outcome had to be detected. Results indicated that temporal recalibration occurred in audition after anodal ctDCS while it was absent in vision. As the adaptation modality was visual, effects in audition suggest that recalibration occurred on a supra-modal level. In active conditions, anodal ctDCS improved sensorimotor recalibration at the delay level closest to the adaptation delay, suggesting a precise cerebellar-dependent temporal recalibration mechanism. In passive conditions, the facilitation of inter-sensory recalibration by anodal ctDCS was overall stronger and tuned to larger delays. These findings point to a role of the cerebellum in supra-modal temporal recalibration across sensorimotor and perceptual domains, but the differential manifestation of the effect across delay levels in active and passive conditions points to differences in the underlying mechanisms depending on the availability of action-based predictions. Furthermore, these results suggest that anodal ctDCS can be a promising tool for facilitating effects of temporal recalibration in sensorimotor and inter-sensory contexts.
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Project description:Combining signals across the senses improves precision and speed of perception, although this multisensory benefit declines for asynchronous signals. Multisensory events may produce synchronized stimuli at source but asynchronies inevitably arise due to distance, intensity, attention and neural latencies. Temporal recalibration is an adaptive phenomenon that serves to perceptually realign physically asynchronous signals. Recently, it was discovered that temporal recalibration occurs far more rapidly than previously thought and does not require minutes of adaptation. Using a classical audiovisual simultaneity task and a series of brief flashes and tones varying in onset asynchrony, perceived simultaneity on a given trial was found to shift in the direction of the preceding trial's asynchrony. Here we examine whether this inter-trial recalibration reflects the same process as prolonged adaptation by combining both paradigms: participants adapted to a fixed temporal lag for several minutes followed by a rapid series of test trials requiring a synchrony judgment. Interestingly, we find evidence of recalibration from prolonged adaptation and inter-trial recalibration within a single experiment. We show a dissociation in which sustained adaptation produces a large but decaying recalibration effect whilst inter-trial recalibration produces large transient effects whose sign matches that of the previous trial.
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Project description:In an ever-changing environment, crossmodal recalibration is crucial to maintain precise and coherent spatial estimates across different sensory modalities. Accordingly, it has been found that perceived auditory space is recalibrated toward vision after consistent exposure to spatially misaligned audio-visual stimuli (VS). While this so-called ventriloquism aftereffect (VAE) yields internal consistency between vision and audition, it does not necessarily lead to consistency between the perceptual representation of space and the actual environment. For this purpose, feedback about the true state of the external world might be necessary. Here, we tested whether the size of the VAE is modulated by external feedback and reward. During adaptation audio-VS with a fixed spatial discrepancy were presented. Participants had to localize the sound and received feedback about the magnitude of their localization error. In half of the sessions the feedback was based on the position of the VS and in the other half it was based on the position of the auditory stimulus. An additional monetary reward was given if the localization error fell below a certain threshold that was based on participants' performance in the pretest. As expected, when error feedback was based on the position of the VS, auditory localization during adaptation trials shifted toward the position of the VS. Conversely, feedback based on the position of the auditory stimuli reduced the visual influence on auditory localization (i.e., the ventriloquism effect) and improved sound localization accuracy. After adaptation with error feedback based on the VS position, a typical auditory VAE (but no visual aftereffect) was observed in subsequent unimodal localization tests. By contrast, when feedback was based on the position of the auditory stimuli during adaptation, no auditory VAE was observed in subsequent unimodal auditory trials. Importantly, in this situation no visual aftereffect was found either. As feedback did not change the physical attributes of the audio-visual stimulation during adaptation, the present findings suggest that crossmodal recalibration is subject to top-down influences. Such top-down influences might help prevent miscalibration of audition toward conflicting visual stimulation in situations in which external feedback indicates that visual information is inaccurate.
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Project description:Recent studies suggest that planned and corrective actions are recalibrated during some forms of motor adaptation. However, corrective (also known as reactive) movements in human locomotion are thought to simply reflect sudden environmental changes independently from sensorimotor recalibration. Thus, we asked whether corrective responses can indicate the motor system's adapted state following prolonged exposure to a novel walking situation inducing sensorimotor adaptation. We recorded electromyographic (EMG) signals bilaterally on 15 leg muscles before, during, and after split-belts walking (i.e., novel walking situation), in which the legs move at different speeds. We exploited the rapid temporal dynamics of corrective responses upon unexpected speed transitions to isolate them from the overall motor output. We found that corrective muscle activity was structurally different following short versus long exposures to split-belts walking. Only after a long exposure, removal of the novel environment elicited corrective muscle patterns that matched those expected in response to a perturbation opposite to the one originally experienced. This indicated that individuals who recalibrated their motor system adopted split-belts environment as their new "normal" and transitioning back to the original walking environment causes subjects to react as if it was novel to them. Interestingly, this learning declined with age, but steady state modulation of muscle activity during split-belts walking did not, suggesting potentially different neural mechanisms underlying these motor patterns. Taken together, our results show that corrective motor commands reflect the adapted state of the motor system, which is less flexible as we age.
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Project description:Neurons in the lateral superior olive (LSO) compute sound location based on differences in interaural intensity, coded in ascending signals from the two cochleas. Unilateral destruction of the neuronal feedback from the LSO to the cochlea, the lateral olivocochlear efferents, disrupted the normal interaural correlation in response amplitudes to sounds of equal intensity. Thus, lateral olivocochlear feedback maintains the binaural balance in neural excitability required for accurate localization of sounds in space.
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Project description:Our sense of relative timing is malleable. For instance, visual signals can be made to seem synchronous with earlier sounds following prolonged exposure to an environment wherein auditory signals precede visual ones. Similarly, actions can be made to seem to precede their own consequences if an artificial delay is imposed for a period, and then removed. Here, we show that our sense of relative timing for combinations of visual changes is similarly pliant. We find that direction reversals can be made to seem synchronous with unusually early colour changes after prolonged exposure to a stimulus wherein colour changes precede direction changes. The opposite effect is induced by prolonged exposure to colour changes that lag direction changes. Our data are consistent with the proposal that our sense of timing for changes encoded by distinct sensory mechanisms can adjust, at least to some degree, to the prevailing environment. Moreover, they reveal that visual analyses of colour and motion are sufficiently independent for this to occur.
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Project description:In the developing auditory system, spontaneous activity generated in the cochleae propagates into the central nervous system to promote circuit formation. The effects of peripheral firing patterns on spontaneous activity in the central auditory system are not well understood. Here, we describe wide-spread bilateral coupling of spontaneous activity that coincides with the period of transient efferent modulation of inner hair cells from the brainstem medial olivocochlear system. Knocking out α9/α10 nicotinic acetylcholine receptors, a requisite part of the efferent pathway, profoundly reduces bilateral correlations. Pharmacological and chemogenetic experiments confirm that the efferent system is necessary for normal bilateral coupling. Moreover, auditory sensitivity at hearing onset is reduced in the absence of pre-hearing efferent modulation. Together, these results demonstrate how afferent and efferent pathways collectively shape spontaneous activity patterns and reveal the important role of efferents in coordinating bilateral spontaneous activity and the emergence of functional responses during the prehearing period.
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Project description:For a comprehensive understanding of the environment, the brain must constantly decide whether the incoming information originates from the same source and needs to be integrated into a coherent percept. This integration process is believed to be mediated by temporal integration windows. If presented with temporally asynchronous stimuli for a few minutes, the brain adapts to this new temporal relation by recalibrating the temporal integration windows. Such recalibration can occur even more rapidly after exposure to just a single trial of asynchronous stimulation. While rapid recalibration has been demonstrated for audio-visual stimuli, evidence for rapid recalibration of visuo-tactile stimuli is lacking. Here, we investigated rapid recalibration in the visuo-tactile domain. Subjects received visual and tactile stimuli with different stimulus onset asynchronies (SOA) and were asked to report whether the visuo-tactile stimuli were presented simultaneously. Our results demonstrate visuo-tactile rapid recalibration by revealing that subjects' simultaneity reports were modulated by the temporal order of stimulation in the preceding trial. This rapid recalibration effect, however, was only significant if the SOA in the preceding trial was smaller than 100 ms, while rapid recalibration could not be demonstrated for SOAs larger than 100 ms. Since rapid recalibration in the audio-visual domain has been demonstrated for SOAs larger than 100 ms, we propose that visuo-tactile recalibration works at shorter SOAs, and thus faster time scales than audio-visual rapid recalibration.
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Project description:Sensorimotor learning critically depends on error signals. Learning usually tries to minimise these error signals to guarantee optimal performance. Errors can, however, have both internal causes, resulting from one's sensorimotor system, and external causes, resulting from external disturbances. Does learning take into account the perceived cause of error information? Here, we investigated the recalibration of internal predictions about the sensory consequences of one's actions. Since these predictions underlie the distinction of self- and externally produced sensory events, we assumed them to be recalibrated only by prediction errors attributed to internal causes. When subjects were confronted with experimentally induced visual prediction errors about their pointing movements in virtual reality, they recalibrated the predicted visual consequences of their movements. Recalibration was not proportional to the externally generated prediction error, but correlated with the error component which subjects attributed to internal causes. We also revealed adaptation in subjects' motor performance which reflected their recalibrated sensory predictions. Thus, causal attribution of error information is essential for sensorimotor learning.
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