Sensory Consequences Of Self-generated Actions Research Articles

Oculomotor corollary discharge signaling is related to repetitive behavior in children with autism spectrum disorder.

Corollary discharge (CD) signals are “copies” of motor signals sent to sensory regions that allow animals to adjust sensory consequences of self-generated actions. Autism spectrum disorder (ASD) is characterized by sensory and motor deficits, which may be underpinned by altered CD signaling. We evaluated oculomotor CD using the blanking task, which measures the influence of saccades on visual perception, in 30 children with ASD and 35 typically developing (TD) children. Participants were instructed to make a saccade to a visual target. Upon saccade initiation, the presaccadic target disappeared and reappeared to the left or right of the original position. Participants indicated the direction of the jump. With intact CD, participants can make accurate perceptual judgements. Otherwise, participants may use saccade landing site as a proxy of the presaccadic target and use it to inform perception. We used multilevel modeling to examine the influence of saccade landing site on trans-saccadic perceptual judgements. We found that, compared with TD participants, children with ASD were more sensitive to target displacement and less reliant on saccade landing site when spatial uncertainty of the post-saccadic target was high. This pattern was driven by ASD participants with less severe restricted and repetitive behaviors. These results suggest a relationship between altered CD signaling and core ASD symptoms.

Predicting the Sensory Consequences of Self-Generated Actions: Pre-Supplementary Motor Area as Supra-Modal Hub in the Sense of Agency Experience.

Sense of agency refers to the feeling that one’s self-generated action caused an external environment event. In a previous study, we suggested that the supplementary motor area (SMA), in its anterior portion (pre-SMA), is a key structure for attributing the sense of agency for the visual consequences of self-generated movements. However, real-life actions can lead to outcomes in different sensory modalities, raising the question of whether SMA represents a supra-modal hub for the sense of agency. Here, we compared the agency experience for visual and auditory outcomes by taking advantage of the intentional binding effect (IB). We observed discrete time-windows for the agency manifestation across different sensory modalities: While there was an IB at 200 ms delay between the action and the visual outcome, a time compression was observed when the auditory outcome followed the action by 400 ms. The magnitude of the IB was mirrored by meaningful brain activity in the pre-SMA but only at the specific delay when a sizeable IB was seen. We conclude that attributing consequences of self-generated movements to one’s action is based on similar mechanisms across sensory modalities and that those mechanisms are related to the functioning of the motor system.

Beta-band oscillations play an essential role in motor-auditory interactions.

In the human brain, self‐generated auditory stimuli elicit smaller cortical responses compared to externally generated sounds. This sensory attenuation is thought to result from predictions about the sensory consequences of self‐generated actions that rely on motor commands. Previous research has implicated brain oscillations in this process. However, the specific role of these oscillations in motor–auditory interactions during sensory attenuation is still unclear. In this study, we aimed at addressing this question by using magnetoencephalography (MEG). We recorded MEG in 20 healthy participants during listening to passively presented and self‐generated tones. Our results show that the magnitude of sensory attenuation in bilateral auditory areas is significantly correlated with the modulation of beta‐band (15–30 Hz) amplitude in the motor cortex. Moreover, we observed a significant directional coupling (Granger causality) in beta‐band originating from the motor cortex toward bilateral auditory areas. Our findings indicate that beta‐band oscillations play an important role in mediating top–down interactions between motor and auditory cortex and, in our paradigm, suppress cortical responses to predicted sensory input.

Schizophrenia and Corollary Discharge: A Neuroscientific Overview and Translational Implications.

Corollary discharge mechanism refers to the suppression of sensory consequences of self-generated actions; a process that serves to distinguish between self and non-self based on discrimination of origination of action. It explains, say for example, why we cannot tickle ourselves. This review discusses how corollary discharge model is an essential neural integration mechanism central to the motor functioning of animal kingdom. In this article, research conducted in the field of corollary discharge has been reviewed to understand the neuroanatomical and neurophysiological basis of corollary discharge and gain insight into the biochemical basis of its dysfunction. This review article also explores the role of corollary discharge and its dysfunction in the presentation of symptoms of schizophrenia, discussing the findings from corollary discharge studies on schizophrenia population. Lastly, the link between schizophrenia psychopathology and corollary discharge dysfunction has been highlighted, and an attempt has been made to establish a case for correction of corollary discharge deficit in schizophrenia through neuromodulation.

Modifying N1 amplitude: Training an expectation that delayed auditory sensations result from a self-initiated action

Event Abstract Back to Event Modifying N1 amplitude: Training an expectation that delayed auditory sensations result from a self-initiated action Ruth B. Elijah1*, Mike E. Le Pelley1 and Thomas J. Whitford1 1 UNSW Australia, Australia Aim: Our ability to suppress self-generated sensations is dependent on the length of time between when an action is initiated and when the resultant sensory information is generated. Specifically, sensations that follow immediately from actions are attenuated to a larger degree than delayed sensations. The current study aimed to determine whether cortical responses to delayed self-initiated auditory events can be modified with training. Method: Electroencephalographic (EEG) recordings where undertaken while participants pressed a button to produce a tone that occurred either immediately or 100ms subsequent to the button-press. The event related potential (ERP) to the tone was generated, and the amplitude of N1 was extracted. Fifty participants were randomly assigned to one of two training groups; one group of participants (n=25) were repeatedly exposed to tones that followed immediately from their button-presses, whereas the other group (n=25) were repeatedly exposed to delayed tones. In order to evaluate the effect of training, participants’ evoked responses to immediate and delayed self-initiated tones were assessed before and after training. Results: Pre-training, the mean amplitude of N1 was significantly larger for delayed tones compared to immediate tones. Participants who were trained to the delayed tones showed a reduction in N1 amplitude across training, such that there was no difference in N1 between immediate and delayed tones post-training. This was in contrast to the participants who received training to immediate tones, who maintained a significantly larger N1 to delayed tones over immediate tones post-training. Conclusions: Repeated exposure to delayed sensory consequences of self-generated actions results in new learning about the temporal relationships between the action and the outcome, and, as such, increased cortical attenuation to temporally delayed sensations. This suggests that behavioural training could represent a potential avenue for alleviating sensory suppression deficits, such as those that have consistently been observed in patients with schizophrenia. References Elijah, R.B., Le Pelley, M.E. & Whitford, T.J. (2016). Modifying temporal expectations: Changing cortical responsivity to delayed self-initiated sensations with training. Biological Psychology, 120, 88-95. Keywords: Sensory Attenuation, N1-suppression, temporal expectation, corollary discharge, event-related potential (ERP) Conference: ASP2016 - The 26th Annual Meeting of the Australasian Society for Psychophysiology, Adelaide Australia, Adelaide,SA, Australia, 12 Dec - 14 Dec, 2016. Presentation Type: Oral Presentation Topic: Abstract (student award) Citation: Elijah RB, Le Pelley ME and Whitford TJ (2016). Modifying N1 amplitude: Training an expectation that delayed auditory sensations result from a self-initiated action. Conference Abstract: ASP2016 - The 26th Annual Meeting of the Australasian Society for Psychophysiology, Adelaide Australia. doi: 10.3389/conf.fnhum.2016.221.00027 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 19 Oct 2016; Published Online: 05 Dec 2016. * Correspondence: Ms. Ruth B Elijah, UNSW Australia, Sydney, NSW, 2052, Australia, ruth.elijah@unsw.edu.au Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Ruth B Elijah Mike E Le Pelley Thomas J Whitford Google Ruth B Elijah Mike E Le Pelley Thomas J Whitford Google Scholar Ruth B Elijah Mike E Le Pelley Thomas J Whitford PubMed Ruth B Elijah Mike E Le Pelley Thomas J Whitford Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Sensory cancellation of self-movement facilitates visual motion detection

The nervous system continuously predicts the sensory consequences of self-generated actions. These predictions can be used to cancel self-generated sensory information. It has been hypothesized that this cancellation process may serve to increase the perceptual sensitivity to unpredicted external events. Here, we provide the first empirical evidence for this idea. Participants were required to detect coherent motion in a random dot motion display. The task was made more difficult by a set of superimposed distractor dots that had to be ignored. When these distractors moved congruently with an active arm movement, perceptual performance in detecting the coherent motion was superior compared to a condition in which the distractor motion did not match the arm movement. To test whether this difference was due to sensory cancellation of matching distractors, or to the attentional enhancement of non-matching distractors, we introduced a control condition without any overt movement. Our results indicate that improvements in the detection of visual motion are indeed caused by sensory cancellation of self-generated events. In conjunction with other recent results, our data therefore suggest that the nervous system is able to attenuate or facilitate self-generated visual stimuli in a task-dependent manner.

Deficits in sensory prediction are related to delusional ideation in healthy individuals

Motor control strongly relies on neural processes that predict the sensory consequences of self-generated actions. Previous research has demonstrated deficits in such sensory-predictive processes in schizophrenic patients and these low-level deficits are thought to contribute to the emergence of delusions of control. Here, we examined the extent to which individual differences in sensory prediction are associated with a tendency towards delusional ideation in healthy participants. We used a force-matching task to quantify sensory-predictive processes, and administered questionnaires to assess schizotypy and delusion-like thinking. Individuals with higher levels of delusional ideation showed more accurate force matching suggesting that such thinking is associated with a reduced tendency to predict and attenuate the sensory consequences of self-generated actions. These results suggest that deficits in sensory prediction in schizophrenia are not simply consequences of the deluded state and are not related to neuroleptic medication. Rather they appear to be stable, trait-like characteristics of an individual, a finding that has important implications for our understanding of the neurocognitive basis of delusions.

Electrophysiological and diffusion tensor imaging evidence of delayed corollary discharges in patients with schizophrenia

Patients with schizophrenia (SZ) characteristically exhibit supranormal levels of cortical activity to self-induced sensory stimuli, ostensibly because of abnormalities in the neural signals (corollary discharges, CDs) normatively involved in suppressing the sensory consequences of self-generated actions. The nature of these abnormalities is unknown. This study investigated whether SZ patients experience CDs that are abnormally delayed in their arrival at the sensory cortex. Twenty-one patients with SZ and 25 matched control participants underwent electroencephalography (EEG). Participants' level of cortical suppression was calculated as the amplitude of the N1 component evoked by a button press-elicited auditory stimulus, subtracted from the N1 amplitude evoked by the same stimulus presented passively. In the three experimental conditions, the auditory stimulus was delivered 0, 50 or 100 ms subsequent to the button-press. Fifteen SZ patients and 17 healthy controls (HCs) also underwent diffusion tensor imaging (DTI), and the fractional anisotropy (FA) of participants' arcuate fasciculus was used to predict their level of cortical suppression in the three conditions. While the SZ patients exhibited subnormal N1 suppression to undelayed, self-generated auditory stimuli, these deficits were eliminated by imposing a 50-ms, but not a 100-ms, delay between the button-press and the evoked stimulus. Furthermore, the extent to which the 50-ms delay normalized a patient's level of N1 suppression was linearly related to the FA of their arcuate fasciculus. These data suggest that SZ patients experience temporally delayed CDs to self-generated auditory stimuli, putatively because of structural damage to the white-matter (WM) fasciculus connecting the sites of discharge initiation and destination.

How do we predict the consequences of our actions? a functional imaging study

Humans are readily able to distinguish expected and unexpected sensory events. Whether a single mechanism underlies this ability is unknown. The most common type of expected sensory events are those generated as a consequence of self-generated actions. Using H 2 15O PET, we studied brain responses to such predictable sensory events (tones) and to similar unpredictable events and especially how the processing of predictable sensory events is modified by the context of a causative self-generated action. Increases in activity when the tones were unpredictable were seen in the inferior and superior temporal lobe bilaterally, the right parahippocampal gyrus and right parietal cortex. Self-generated actions produced activity in a number of motor and premotor areas, including dorsolateral prefrontal cortex. We observed an interaction between the predictability of stimuli and self-generated actions in several areas, including the medial posterior cingulate cortex, left insula, dorsomedial thalamus, superior colliculus and right inferior temporal cortex. This modulation of activity associated with stimulus predictability in the context of self-generated actions implies that these areas may be involved in self-monitoring processes. Detection of expected stimuli and the detection of the sensory consequences of self-generated actions appear to be functionally distinct processes, and are carried out in different cortical areas. These observations support theoretical approaches to cognition that postulate the existence of a self-monitoring system.