Relationship between cardiac cycle and the timing of actions during action execution and observation.

Previous research suggests that there may be a relationship between the timing of motor events and phases of the cardiac cycle. This relationship has thus far only been researched using simple isolated movements such as key-presses in reaction-time tasks and only in a single subject acting alone. Other research has shown both movement and cardiac coordination among interacting individuals. Here, we investigated how the cardiac cycle relates to ongoing self-paced movements in both action execution and observation using a novel dyadic paradigm. We recorded electrocardiography (ECG) in 26 subjects who formed 19 dyads containing an action executioner and observer as they performed a self-paced sequence of movements. We demonstrated that heartbeats are timed to movements during both action execution and observation. Specifically, movements were less likely to culminate synchronously with the heartbeat around the time of the R-peak of the ECG. The same pattern was observed for action observation, with the observer's heartbeats occurring off-phase with movement culmination. These findings demonstrate that there is coordination between an action executioner's cardiac cycle and the timing of their movements, and that the same relationship is mirrored in an observer. This suggests that previous findings of interpersonal coordination may be caused by the mirroring of a phasic relationship between movement and the heart.

Dissociation in How Core Autism Features Relate to Interoceptive Dimensions: Evidence from Cardiac Awareness in Children.

Interoception in autism is receiving increasing research attention. Previously, differences were identified in autism on both objective and subjective measures of interoception, and an association with anxiety. Yet, it is currently unknown how interoception relates to core autism features. Here, in 49 autistic children, we consider how interoceptive accuracy (measured with heartbeat detection tasks) and sensibility (subjective judgements of awareness) relate to overall severity on the Autism Diagnostic Observation Schedule, and symptom domains of social-affective and repetitive, restricted behaviors. Socio-affective features were related to interoceptive sensibility, while repetitive restricted behaviors were related to interoceptive accuracy. This dissociation suggests disparate interoceptive mechanisms for the formation and/or maintenance of autistic features.

The link between interoceptive processing and anxiety in children diagnosed with autism spectrum disorder: Extending adult findings into a developmental sample.

Anxiety is a major associated feature of autism spectrum disorders. The incidence of anxiety symptoms in this population has been associated with altered interoceptive processing. Here, we investigated whether recent findings of impaired interoceptive accuracy (quantified using heartbeat detection tasks) and exaggerated interoceptive sensibility (subjective sensitivity to internal sensations on self-report questionnaires) in autistic adults, can be extended into a school-age sample of children and adolescents (n = 75). Half the sample had a verified diagnosis of an Autism Spectrum Disorder (ASD) and half were IQ- and age-matched children and adolescents without ASD. The discrepancy between an individual's score on these two facets of interoception (interoceptive accuracy and interoceptive sensibility), conceptualized as an interoceptive trait prediction error, was previously found to predict anxiety symptoms in autistic adults. We replicated the finding of reduced interoceptive accuracy in autistic participants, but did not find exaggerated interoceptive sensibility relative to non-autistic participants. Nonetheless, the positive association between anxiety and interoceptive trait prediction error was replicated. However, in this sample, the best predictor of anxiety symptoms was interoceptive sensibility. Finally, we observed lower metacognitive accuracy for interoception in autistic children and adolescents, relative to their non-autistic counterparts. Despite their reduced interoceptive accuracy on the heartbeat tracking task and comparable accuracy on the heartbeat discrimination task, the autistic group reported higher confidence than the typical group in the discrimination task. Findings are consistent with theories of ASD as a disorder of interoceptive processing, but highlight the importance of validating cognitive models of developmental conditions within developmental populations.

Altering movement parameters disrupts metacognitive accuracy.

Correctly estimating the confidence we should have in our decisions has traditionally been viewed as a perceptual judgement based solely on the strength or quality of sensory information. However, accumulating evidence has demonstrated that the motor system contributes to judgements of perceptual confidence. Here, we manipulated the speed at which participants' moved using a behavioural priming task and showed that increasing movement speed above participants' baseline measures disrupts their ability to form accurate confidence judgements about their performance. Specifically, after being primed to move faster than they would naturally, participants reported higher confidence in their incorrect decisions than when they moved at their natural pace. We refer to this finding as the adamantly wrong effect. The results are consistent with the hypothesis that veridical feedback from the effector used to indicate a decision is employed to form accurate metacognitive judgements of performance.

Abnormal movement-related suppression of sensory evoked potentials in upper limb dystonia.

BACKGROUND: Gating of sensory evoked potentials (SEPs) around the onset of a voluntary movement is a physiological phenomenon with centripetal and central components, and may reflect sensorimotor integration required for normal movement control. OBJECTIVE: Our objective was the investigation of SEP suppression at the onset of movement and the interaction between SEP suppression and vibration of the limb. METHODS: Fourteen patients with primary focal/segmental dystonia and 17 age-matched healthy volunteers were studied. SEPs were elicited after electrical stimulation of the median nerve at the wrist. Electroencephalograms (EEGs) were recorded over the scalp at three sites according to the International 10-20 System (F3, C3 and P3). SEPs were recorded in four conditions: at rest, at the onset of movement (a self-paced abduction movement of the right thumb), both in the absence and in the presence of vibration of the limb. RESULTS: Repeated measures anova revealed that there was a significant main effect of group [F(1, 11.1) = 0.471, P = 0.002]. Post hoc exploration of this effect revealed it to be due to an absence of SEP suppression at movement onset in patients (mean ratio SEP movement onset/rest 1.15 at F3, 1.13 at C3, 1.01 at P3) compared to controls, who had SEP suppression at movement onset (mean ratio SEP movement onset/rest 0.79 at F3, 0.78 at C3, 0.77 at P3). With vibration, SEP suppression reduced in both patients and controls to a similar extent. CONCLUSION: These results demonstrate abnormal SEP suppression at the onset of movement in patients with primary dystonia, and in addition that vibration of the limb reduces SEP suppression in patients and controls.

Linking differences in action perception with differences in action execution.

Successful human social interactions depend upon the transmission of verbal and non-verbal signals from one individual to another. Non-verbal social communication is realized through our ability to read and understand information present in other people's actions. It has been proposed that employing the same motor programs, we use to execute an action when observing the same action underlies this action understanding. The main prediction of this framework is that action perception should be strongly correlated with parameters of action execution. Here, we demonstrate that subjects' sensitivity to observed movement speeds is dependent upon how quickly they themselves executed the observed action. This result is consistent with the motor theory of social cognition and suggests that failures in non-verbal social interactions between individuals may in part result from differences in how those individuals move.

Do monkey F5 mirror neurons show changes in firing rate during repeated observation of natural actions?

Mirror neurons were first discovered in area F5 of macaque monkeys. In humans, noninvasive studies have demonstrated an increased blood oxygen level-dependent (BOLD) signal in homologous motor areas during action observation. One approach to demonstrating that this indicates the existence of mirror neurons in humans has been to employ functional (f)MRI adaptation to test whether the same population of neurons is active during both observation and execution conditions. Although a number of human studies have reported fMRI adaptation in these areas, a recent study has shown that macaque mirror neurons do not attenuate their firing rate with two repetitions. Here we investigated whether mirror neurons modulate their firing rate when monkeys observed the same repeated natural action multiple times. We recorded from 67 mirror neurons in area F5 of two macaque monkeys while they observed an experimenter perform a reach-to-grasp action on a small food reward using a precision grip. Although no changes were detectable for the first two repetitions, we show that both the firing rate and the latency at which mirror neurons discharged during observation were subtly modulated by the repetition of the observed action over 7-10 trials. Significant adaption was mostly found in the period immediately before the grasp was performed. We also found that the local field potential activity in F5 (beta-frequency range, 16-23 Hz), which is attenuated during action observation, also showed systematic changes with repeated observation. These LFP changes occurred well in advance of the mirror neuron adaptation. We conclude that macaque mirror neurons can show intra-modal adaptation, but whether this is related to fMRI adaptation of the BOLD signal requires further investigation.

What we know currently about mirror neurons.

Mirror neurons were discovered over twenty years ago in the ventral premotor region F5 of the macaque monkey. Since their discovery much has been written about these neurons, both in the scientific literature and in the popular press. They have been proposed to be the neuronal substrate underlying a vast array of different functions. Indeed so much has been written about mirror neurons that last year they were referred to, rightly or wrongly, as "The most hyped concept in neuroscience". Here we try to cut through some of this hyperbole and review what is currently known (and not known) about mirror neurons.

Inferring subjective states through the observation of actions.

Estimating another person's subjective confidence is crucial for social interaction, but how this inference is achieved is unknown. Previous research has demonstrated that the speed at which people make decisions is correlated with their confidence in their decision. Here, we show that (i) subjects are able to infer the subjective confidence of another person simply through the observation of their actions and (ii) this inference is dependent upon the performance of each subject when executing the action. Crucially, the latter result supports a model in which motor simulation of an observed action mediates the successful understanding of other minds. We conclude that kinematic understanding allows access to the higher-order cognitive processes of others, and that this access plays a central role in social interactions.

Role of the parietal cortex in predicting incoming actions.

Animal and human studies have shown that the parietal and the ventral premotor cortices constitute the neural substrate of the so-called mirror system. The word "mirror" originally referred to the discovery of neurons in non-human primates whose visual response echoes their motor response. This account proposes that action understanding and imitation depend on a mechanism which activates directly our own motor system as we observe the actions of other agents (Rizzolatti and Sinigaglia, 2010). Single unit recording experiments have also demonstrated that parietal neurons have predictive activity and discharge well ahead of a planned movement. Interestingly, patients with parietal damage can show impairments in their ability to imitate or understand an observed action, but they have also difficulties in monitoring early phases of their own movement planning, be it simple reaching movements or more complex object-directed actions. The fact that both deficits may co-occur after a parietal lesion raises the question whether this reflects the impairment of a common mechanism. To address this question we examined EEG activity in patients with selective lesions in the inferior parietal lobe (N=6) who were requested to watch passively a video showing an actor grasping a colored object. The object's color cued the subject that the actor was about to move. We recorded the Readiness Potential (RP), a marker of motor preparation which also arises when preparing to observe an action (Kilner et al., 2004). Parietal patients' performance was compared to that of neurologically normal subjects (n=9) and patients with a ventral premotor cortex lesion (N=4). We show that neurologically normal subjects and premotor patients exhibit a significant RP prior to the observed action, whereas no such RP is observed in parietal patients. Our results indicate that parietal cortex injury alters the ability to monitor the early planning phases not only of one's own actions but those of other agents as well. We speculate that parietal activity during action observation does not only or essentially reflect a mirroring process, as recently proposed by mirror neurons' account, but involve instead an anticipatory process which arises through prior learning and predictive mechanisms.

Changing meaning causes coupling changes within higher levels of the cortical hierarchy.

Processing of speech and nonspeech sounds occurs bilaterally within primary auditory cortex and surrounding regions of the superior temporal gyrus; however, the manner in which these regions interact during speech and nonspeech processing is not well understood. Here, we investigate the underlying neuronal architecture of the auditory system with magnetoencephalography and a mismatch paradigm. We used a spoken word as a repeating "standard" and periodically introduced 3 "oddball" stimuli that differed in the frequency spectrum of the word's vowel. The closest deviant was perceived as the same vowel as the standard, whereas the other 2 deviants were perceived as belonging to different vowel categories. The neuronal responses to these vowel stimuli were compared with responses elicited by perceptually matched tone stimuli under the same paradigm. For both speech and tones, deviant stimuli induced coupling changes within the same bilateral temporal lobe system. However, vowel oddball effects increased coupling within the left posterior superior temporal gyrus, whereas perceptually equivalent nonspeech oddball effects increased coupling within the right primary auditory cortex. Thus, we show a dissociation in neuronal interactions, occurring at both different hierarchal levels of the auditory system (superior temporal versus primary auditory cortex) and in different hemispheres (left versus right). This hierarchical specificity depends on whether auditory stimuli are embedded in a perceptual context (i.e., a word). Furthermore, our lateralization results suggest left hemisphere specificity for the processing of phonological stimuli, regardless of their elemental (i.e., spectrotemporal) characteristics.

Forward and backward connections in the brain: a DCM study of functional asymmetries.

In this paper, we provide evidence for functional asymmetries in forward and backward connections that define hierarchical architectures in the brain. We exploit the fact that modulatory or nonlinear influences of one neuronal system on another (i.e., effective connectivity) entail coupling between different frequencies. Functional asymmetry in forward and backward connections was addressed by comparing dynamic causal models of MEG responses induced by visual processing of normal and scrambled faces. We compared models with and without nonlinear (between-frequency) coupling in both forward and backward connections. Bayesian model comparison indicated that the best model had nonlinear forward and backward connections. Using the best model we then quantified frequency-specific causal influences mediating observed spectral responses. We found a striking asymmetry between forward and backward connections; in which high (gamma) frequencies in higher cortical areas suppressed low (alpha) frequencies in lower areas. This suppression was significantly greater than the homologous coupling in the forward connections. Furthermore, exactly the asymmetry was observed when we examined face-selective coupling (i.e., coupling under faces minus scrambled faces). These results highlight the importance of nonlinear coupling among brain regions and point to a functional asymmetry between forward and backward connections in the human brain that is consistent with anatomical and physiological evidence from animal studies. This asymmetry is also consistent with functional architectures implied by theories of perceptual inference in the brain, based on hierarchical generative models.

Neural correlates of perceptual filling-in of an artificial scotoma in humans.

When a uniformly illuminated surface is placed eccentrically on a dynamic textured background, after a few seconds, it is perceived to disappear and be replaced by the background texture. Such texture filling-in is thought to occur in retinotopic visual cortex, but it has proven difficult to distinguish the contributions of invisible target and visible background to signals measured in these areas. Here, we used magnetoencephalography to measure time-dependent brain responses in human observers experiencing texture completion. We measured responses specifically associated with the filled-in target, by isolating neural population signals entrained at the frequency of flicker of the target. When perceptual completion occurred, and the target became invisible, there was significant reduction in the magnetoencephalography power at the target frequency over contralateral posterior sensors. However, even a subjectively invisible target nevertheless evoked frequency-specific signals compared with a no-target baseline. These data represent evidence for a persistent target-specific representation even for stimuli rendered invisible because of perceptual filling-in.

Hemodynamic correlates of EEG: a heuristic.

In this note we describe a heuristic, starting with a dimensional analysis, which relates hemodynamic changes to the spectral profile of ongoing EEG activity. In brief, this analysis suggests that 'activation', as indexed by increases in hemodynamic signals, should be associated with a loss of power in lower EEG frequencies, relative to higher frequencies. The fact that activation is expressed in terms of frequency (i.e., per second) is consistent with a dimensional analysis in the sense that activations reflect the rate of energy dissipation (per second). In this heuristic, activation causes an acceleration of temporal dynamics leading to (i) increased energy dissipation; (ii) decreased effective membrane time constants; (iii) increased effective coupling among neuronal ensembles; and (iv) a shift in the EEG spectral profile to higher frequencies. These predictions are consistent with empirical observations of how changes in the EEG spectrum are expressed hemodynamically. Furthermore, the heuristic provides a simple measure of neuronal activation based on spectral analyses of EEG.

Coupling of oscillatory activity between muscles is strikingly reduced in a deafferented subject compared with normal controls.

Oscillatory activity in the primate motor cortex has been shown to be phase locked to oscillations in contralateral hand and forearm muscle activity in the 15- to 30-Hz frequency range. Recent studies have shown that the degree of coupling between the cortex and the periphery is strongly influenced by the type and degree of movements of the digits. It has also been suggested that changes in corticomuscular and muscle-muscle coherence could be modulated by peripheral sensory inputs. In the current study, we investigated task-dependent changes in the coherent coupling of electromyographic (EMG) activity recorded from different intrinsic (abductor pollicis brevis and first dorsal interosseous) and two extrinsic (flexor digitorum superficialis and extensor digitorum communis) hand muscles during performance of a precision-grip task by normal subjects and by a single subject who has a total loss of touch, vibration, pressure, and kinesthetic sensation below the neck. The task required a hold-move-hold pattern of grip force to be exerted on a compliant object with the dominant right hand. We found significant task-related modulation of 15- to 30-Hz coherence between EMG activity in hand muscles in the control subjects. In contrast, the deafferented subject showed very low levels of significant coherence in the 15- to 30-Hz range and no peak at this frequency in the power spectra of her EMG activity. These results suggest that the presence of sensory afferent signals are necessary for the modulation of 15- to 30-Hz oscillations in the motor system.

An interference effect of observed biological movement on action.

It has been proposed that actions are intrinsically linked to perception and that imagining, observing, preparing, or in any way representing an action excites the motor programs used to execute that same action. There is neurophysiological evidence that certain brain regions involved in executing actions are activated by the mere observation of action (the so-called "mirror system;" ). However, it is unknown whether this mirror system causes interference between observed and simultaneously executed movements. In this study we test the hypothesis that, because of the overlap between action observation and execution, observed actions should interfere with incongruous executed actions. Subjects made arm movements while observing either a robot or another human making the same or qualitatively different arm movements. Variance in the executed movement was measured as an index of interference to the movement. The results demonstrate that observing another human making incongruent movements has a significant interference effect on executed movements. However, we found no evidence that this interference effect occurred when subjects observed a robotic arm making incongruent movements. These results suggest that the simultaneous activation of the overlapping neural networks that process movement observation and execution infers a measurable cost to motor control.

Task-dependent modulations of cortical oscillatory activity in human subjects during a bimanual precision grip task.

Oscillations are a widespread feature of normal brain activity and have been reported at a variety of different frequencies in different neuronal systems. The demonstration that oscillatory activity is present in motor command signals has prompted renewed interest in the possible functions of synchronous oscillatory activity within the primate sensorimotor system. In the current study, we investigated task-dependent modulations in coupling between sensorimotor cortical oscillators during a bimanual precision grip task. The task required a hold-ramp-hold pattern of grip force to be exerted on a compliant object with the dominant right hand, while maintaining a steady grip with the nondominant hand. We found significant task-related modulation of 15- to 30-Hz coherence between magnetoencephalographic (MEG) activity recorded from the left sensorimotor cortex and electromyographic (EMG) activity in hand muscles on the right side. This coherence was maximal during steady hold, but disappeared during the ramp movements. Interestingly coherence between the right sensorimotor MEG and left-hand EMG showed a similar, although less deeply modulated, task-related pattern, even though this hand was maintaining a simple steady grip. No significant ipsilateral MEG-EMG coherence was observed in the 15- to 30-Hz passband for either hand. These results suggest that the cortical oscillators in the two sensorimotor cortices are independent to some degree but that they may share a common mechanism that attenuates the cortical power in both hemispheres in the 15- to 30-Hz range during movements of one hand. The results are consistent with the hypothesis that oscillatory activity in the motor system is important in resetting the descending motor commands needed for changes in motor state, such as those that occur in the transition from movement to steady grip.

Modulation of synchrony between single motor units during precision grip tasks in humans.

During precision grip, coherence between motor cortex and hand muscle EMG oscillatory activity in the 15-30 Hz range covaries with the compliance of the manipulated object. The current study investigated whether short-term synchrony and coherence between discharges of single motor units (SMUs) in the first dorsal interosseous (1DI) muscle were similarly modulated by object compliance during precision grip. Eight subjects used index finger and thumb to grip two levers that were under robotic control. Guided by visual feedback of the lever force levels, subjects held the levers against a steady force of 1.3 N for 8 s; they then linearly increased the force to 1.6 N over a 2 s period and held for a further 8 s before linearly decreasing the force back to the 1.3 N level over another 2 s period. Subjects performed the task at two different levels of compliance, each with identical grip force levels. Both surface EMG and SMU activity were recorded from the 1DI muscle. Short-term synchrony between the discharges of pairs of SMUs was assessed in the time domain by cross-correlation and in the frequency domain by coherence analysis. Coherence was seen in two frequency ranges: 6-12 Hz and 15-30 Hz. The compliance of the gripped object had a significant effect on both short-term synchronisation and coherence in the 15-30 Hz range between SMUs; both were greater for the more compliant condition. There was no change in the 6-12 Hz coherence.