Predictive and retrospective association of action and sensory feedback in healthy subjects and clinical disorders of the sense of agency(renewal proposal as part of the project "Neural coding of causality in instrumental behavior")
Final Report Abstract
Humans have little difficulty distinguishing changes in the external world that are due to their own actions from those that are not. However, this “sense of agency” may be inaccurate: Over- or underestimation of control is a feature of several neuropsychiatric disorders. During my funding period at the Wellcome Trust Centre for Neuroimaging at University College London, I examined how different aspects of subjective agency are related to instrumental control processes. When sensory input is the result of acting, its perceived intensity is attenuated. This is often taken as evidence for an action-specific sensory prediction mechanism, based on an efference copy of the motor command. To test this action-specificity, we developed a perceptual metric of sensory attenuation that is independent of the more general perceptual effects of stimulus predictability and attention. This de-confounded metric correlates with motor processes during action selection, in support of its action-specificity. Combining this perceptual paradigm with magnetoencephalography, we observed an anticipatory modulation in sensory cortex during action preparation. This sensory modulation emerges at a time when effector selection is ongoing, favouring parallel processing streams for motor output and sensory prediction rather than a general efference-based prediction mechanism. Another implicit effect of agency on perception is an attraction of the perceived time of one’s own voluntary actions and consequent sensory input ("temporal binding"; Haggard et al., 2002). Using exploratory factor analysis of a large behavioural data set across a battery of decision-making and agency tasks, we could dissociate two components of temporal binding. Individuals whose actions strongly biased perception of subsequent consequences displayed poor exploitation of their own instrumentality. Inaccurate action awareness, on the other hand, was associated with psychomotor efficiency. These findings reveal interactions between subjective agency and action control which are hidden when both are studied in isolation. We are currently testing the same task battery in Parkinson’s Disease (PD) patients with medication-induced impulse control disorders (ICD). These are side effects of dopaminergic treatment which could, in principle, result from an overestimation of an agent’s own control. We are also testing whether deep brain stimulation (DBS), another therapy for PD that can lead to ICD, causes similar changes to the sense of agency. During my funding period, I became more and more interested in the role the nucleus accumbens (Nacc) plays in action selection. This interest was partly motivated by a focus of my host institute on decision-making, partly by an emerging role of the Nacc for DBS in neuropsychiatric disorders. Based on rare electrophysiological data recorded from DBS electrodes in the Nacc of epilepsy patients, we tested for two fundamental aspects of Nacc processing. As predicted from rodent work, we observed a cortical drive of low-frequency oscillations in the human Nacc during instrumental action. In a second study, we found no evidence of a unified reward prediction error (RPE) in local field potentials from the human Nacc, which contrasts with RPE signals in neuronal firing or human fMRI. Taken together, I have tested important, experimentally elusive aspects of a sense of agency, both in healthy humans and neurological patients. In addition, I have developed a second research interest in basal ganglia function in action control. I am planning to pursue both of these interests by studying neuropsychiatric disorders with a focus on DBS.
Publications
- (2014). Enhanced Alpha-oscillations in Visual Cortex during Anticipation of Self-generated Visual Stimulation. Journal of Cognitive Neuroscience, 2540–2551
Stenner, M.-P., Bauer, M., Haggard, P., Heinze, H.-J., & Dolan, R.
(See online at https://doi.org/10.1162/jocn_a_00658) - (2014). Reconstruction of action awareness depends on an internal model of action-outcome timing. Consciousness and Cognition, 25, 11–16
Stenner, M.-P., Bauer, M., Machts, J., Heinze, H.-J., Haggard, P., & Dolan, R. J.
(See online at https://dx.doi.org/10.1016%2Fj.concog.2014.01.007) - (2014). Subliminal action priming modulates the perceived intensity of sensory action consequences. Cognition, 130(2), 227–235
Stenner, M.-P., Bauer, M., Sidarus, N., Heinze, H.-J., Haggard, P., & Dolan, R. J.
(See online at https://doi.org/10.1016/j.cognition.2013.11.008) - (2015). Parallel processing streams for motor output and sensory prediction during action preparation. Journal of Neurophysiology, 113(6), 1752-1762
Stenner, M.-P., Bauer, M., Heinze, H.-J., Haggard, P., & Dolan, R. J.
(See online at https://doi.org/10.1152/jn.00616.2014)
