Eamonn Walsh

Automatic Imitation of Intransitive Actions.

Previous research has indicated a potential discontinuity between monkey and human ventral premotor-parietal mirror systems, namely that monkey mirror systems process only transitive (object-directed) actions, whereas human mirror systems may also process intransitive (non-object-directed) actions. The present study investigated this discontinuity by seeking evidence of automatic imitation of intransitive actions--hand opening and closing--in humans using a simple reaction time (RT), stimulus-response compatibility paradigm. Left-right and up-down spatial compatibility were controlled by ensuring that stimuli were presented and responses executed in orthogonal planes, and automatic imitation was isolated from simple and complex orthogonal spatial compatibility by varying the anatomical identity of the stimulus hand and response hemispace, respectively. In all conditions, action compatible responding was faster than action incompatible responding, and no effects of spatial compatibility were observed. This experiment therefore provides evidence of automatic imitation of intransitive actions, and support for the hypothesis that human and monkey mirror systems differ with respect to the processing of intransitive actions.

Experience of agency and sense of responsibility

The experience of agency refers to the feeling that we control our own actions, and through them the outside world. In many contexts, sense of agency has strong implications for moral responsibility. For example, a sense of agency may allow people to choose between right and wrong actions, either immediately, or on subsequent occasions through learning about the moral consequences of their actions. In this study we investigate the relation between the experience of operant action, and responsibility for action outcomes using the intentional binding effect (Haggard, Clark, & Kalogeras, 2002) as an implicit, quantitative measure related to sense of agency. We studied the time at which people perceived simple manual actions and their effects, when these actions were embedded in scenarios where their actions had unpredictable consequences that could be either moral or merely economic. We found an enhanced binding of effects back towards the actions that caused them, implying an enhanced sense of agency, in moral compared to non-moral contexts. We also found stronger binding for effects with severely negative, compared to moderately negative, values. A tight temporal association between action and effect may be a low-level phenomenal marker of the sense of responsibility.

The functional anatomy of suggested limb paralysis.

Suggestions of limb paralysis in highly hypnotically suggestible subjects have been employed to successfully model conversion disorders, revealing similar patterns of brain activation associated with attempted movement of the affected limb. However, previous studies differ with regard to the executive regions involved during involuntary inhibition of the affected limb. This difference may have arisen as previous studies did not control for differences in hypnosis depth between conditions and/or include subjective measures to explore the experience of suggested paralysis. In the current study we employed functional magnetic resonance imaging (fMRI) to examine the functional anatomy of left and right upper limb movements in eight healthy subjects selected for high hypnotic suggestibility during (i) hypnosis (NORMAL) and (ii) attempted movement following additional left upper limb paralysis suggestions (PARALYSIS). Contrast of left upper limb motor function during NORMAL relative to PARALYSIS conditions revealed greater activation of contralateral M1/S1 and ipsilateral cerebellum, consistent with the engagement of these regions in the completion of movements. By contrast, two significant observations were noted in PARALYSIS relative to NORMAL conditions. In conjunction with reports of attempts to move the paralysed limb, greater supplementary motor area (SMA) activation was observed, a finding consistent with the role of SMA in motor intention and planning. The anterior cingulate cortex (ACC, BA 24) was also significantly more active in PARALYSIS relative to NORMAL conditions - suggesting that ACC (BA 24) may be implicated in involuntary, as well as voluntary inhibition of prepotent motor responses.

EEG activations during intentional inhibition of voluntary action: An electrophysiological correlate of self­control?

An important aspect of volition is the internal decision whether to act or to withhold an action. We used EEG frequency analysis of sensorimotor rhythms to investigate brain activity when people prepare and then cancel a voluntary action. Participants used a rotating clock-hand to report when they experienced the intention to press a key with their right hand, even on trials where they freely decided to inhibit movement at the last moment. On action trials, we observed the classical pattern of reduced beta-band spectral power prior to movement, followed by beta rebound after movement. On inhibition trials where participants prepared but then cancelled a movement, we found a left frontal increase in spectral power (event-related synchronisation: ERS) peaking 12 ms before the perceived intention to move. This neural correlate of intentional inhibition was significantly different from the activity at the corresponding moment in action trials. The results are discussed in the context of a recent model of voluntary action (WWW model; Brass & Haggard, 2008). Planned actions can be subjected to a final predictive check which either commits actions for execution or suspends and withholds them. The neural mechanism of intentional inhibition may play an important role in self-control.

Modelling psychiatric and cultural possession phenomena with suggestion and fMRI

Involuntary movements occur in a variety of neuropsychiatric disorders and culturally influenced dissociative states (e.g., delusions of alien control and attributions of spirit possession). However, the underlying brain processes are poorly understood. We combined suggestion and fMRI in 15 highly hypnotically susceptible volunteers to investigate changes in brain activity accompanying different experiences of loss of self-control of movement. Suggestions of external personal control and internal personal control over involuntary movements modelled delusions of control and spirit possession respectively. A suggestion of impersonal control by a malfunctioning machine modelled technical delusions of control, where involuntary movements are attributed to the influence of machines. We found that (i) brain activity and/or connectivity significantly varied with different experiences and attributions of loss of agency; (ii) compared to the impersonal control condition, both external and internal personal alien control were associated with increased connectivity between primary motor cortex (M1) and brain regions involved in attribution of mental states and representing the self in relation to others; (iii) compared to both personal alien control conditions, impersonal control of movement was associated with increased activity in brain regions involved in error detection and object imagery; (iv) there were no significant differences in brain activity, and minor differences in M1 connectivity, between the external and internal personal alien control conditions. Brain networks supporting error detection and object imagery, together with representation of self and others, are differentially recruited to support experiences of impersonal and personal control of involuntary movements. However, similar brain systems underpin attributions and experiences of external and internal alien control of movement. Loss of self-agency for movement can therefore accompany different kinds of experience of alien control supported by distinct brain mechanisms. These findings caution against generalization about single cognitive processes or brain systems underpinning different experiences of loss of self-control of movement.

Using hypnotic suggestion to model loss of control and awareness of movements: an exploratory FMRI study.

The feeling of voluntary control and awareness of movement is fundamental to our notions of selfhood and responsibility for actions, yet can be lost in neuropsychiatric syndromes (e.g. delusions of control, non-epileptic seizures) and culturally influenced dissociative states (e.g. attributions of spirit possession). The brain processes involved remain poorly understood. We used suggestion and functional magnetic resonance imaging (fMRI) to investigate loss of control and awareness of right hand movements in 15 highly hypnotically suggestible subjects. Loss of perceived control of movements was associated with reduced connectivity between supplementary motor area (SMA) and motor regions. Reduced awareness of involuntary movements was associated with less activation in parietal cortices (BA 7, BA 40) and insula. Collectively these results suggest that the sense of voluntary control of movement may critically depend on the functional coupling of SMA with motor systems, and provide a potential neural basis for the narrowing of awareness reported in pathological and culturally influenced dissociative phenomena.

Representing the consequences of intentionally inhibited actions

The experience of planning an action but then changing our minds and cancelling the action at the last instant is a common one. Here, we instructed participants to prepare voluntary (keypress) actions and sometimes intentionally inhibit them at the last possible moment. Participants could freely choose between left and right hand actions. Keypresses produced either a congruent (80% probability) or an incongruent (20% probability) tone after a short delay. If no voluntary action was made within a defined response window, one of the tones was nevertheless presented a short time later. At the end of the trial, participants judged the time of tone onset. We used an established marker to measure the experience of control, namely the intentional binding of the tone backwards in time towards the action that caused it. Results showed that voluntary actions produced the expected temporal binding of tones back towards the preceding action. In contrast, we found an opposite trend towards repulsion of the tone in intentional inhibition trials. When people intentionally inhibit a planned action, their experience of a subsequent event that was associated with the action is severely affected. Our results suggest that intentional inhibition is a specific cognitive process that strongly influences action prediction and action experience.

The functional anatomy and connectivity of thought insertion and alien control of movement

Alien control phenomena are symptoms reported by patients with schizophrenia whereby feelings of control and ownership of thoughts and movements are lost. Comparable alien control experiences occur in culturally influenced dissociative states. We used fMRI and suggestions for automatic writing in highly hypnotically suggestible individuals to investigate the neural underpinnings of alien control. Targeted suggestions selectively reduced subjective ratings of control and ownership for both thought and movement. Thought insertion (TI) was associated with reduced activation of networks supporting language, movement, and self-related processing. In contrast, alien control of writing movement was associated with increased activity of a left-lateralised cerebellar-parietal network and decreased activity in brain regions involved in voluntary movement, including sensory-motor hand areas and the thalamus. Both experiences involved a reduction in activity of left supplementary motor area (SMA) and were associated with altered functional connectivity (FC) between SMA and brain regions involved in language processing and movement implementation. Collectively these results indicate the SMA plays a central role in alien control phenomena as a high level executive system involved in the sense that we control and own our thoughts and movements.

The effects of acoustic startle on sensorimotor attenuation prior to movement

A startling auditory stimulus delivered unexpectedly can activate subcortical structures triggering a prepared movement involuntarily and shortening reaction times. We investigated the effects of the startle acceleration of response on sensory suppression, a phenomenon linked to the voluntary motor command whereby a tactile stimulus is less likely to be perceived on a moving body-part prior to voluntary movement than at rest. Subjects had to detect weak shocks which were delivered to the index finger after a Go signal on some trials. We found that detection rates on movement trials were lower than on non-movement trials, consistent with sensory suppression. In addition, a loud acoustic stimulus was presented at the same time as the Go signal on some trials (startle trials). Reaction times were significantly shorter on startle trials than on other trials, replicating previous startle acceleration of reaction time effects attributed to the operation of subcortical pathways. However, we found no overall difference in premovement sensory suppression effects between baseline and startle movement trials. Rather, startle acceleration of voluntary reactions produced a corresponding acceleration of sensory suppression. Our results provide evidence for a subcortical contribution to sensory suppression and suggest that sensory suppression is a highly general form of motor and sensory interaction.

An investigation of regional cerebral blood flow and tissue structure changes after acute administration of antipsychotics in healthy male volunteers

Chronic administration of antipsychotic drugs has been linked to structural brain changes observed in patients with schizophrenia. Recent MRI studies have shown rapid changes in regional brain volume following just a single dose of these drugs. However, it is not clear if these changes represent real volume changes or are artefacts (“apparent” volume changes) due to drug‐induced physiological changes, such as increased cerebral blood flow (CBF). To address this, we examined the effects of a single, clinical dose of three commonly prescribed antipsychotics on quantitative measures of T1 and regional blood flow of the healthy human brain. Males (n = 42) were randomly assigned to one of two parallel groups in a double‐blind, placebo‐controlled, randomized, three‐period cross‐over study design. One group received a single oral dose of either 0.5 or 2 mg of risperidone or placebo during each visit. The other received olanzapine (7.5 mg), haloperidol (3 mg), or placebo. MR measures of quantitative T1, CBF, and T1‐weighted images were acquired at the estimated peak plasma concentration of the drug. All three drugs caused localized increases in striatal blood flow, although drug and region specific effects were also apparent. In contrast, all assessments of T1 and brain volume remained stable across sessions, even in those areas experiencing large changes in CBF. This illustrates that a single clinically relevant oral dose of an antipsychotic has no detectable acute effect on T1 in healthy volunteers. We further provide a methodology for applying quantitative imaging methods to assess the acute effects of other compounds on structural MRI metrics. Hum Brain Mapp 39:319–331, 2018.