Dissociating What and When of Intentional Actions

Recent brain imaging research revealed that internally guided actions involve the frontomedian wall, in particular the preSMA and the rostral cingulate zone (RCZ). However, a systematic decomposition of different components of intentional action is still lacking. We propose a new paradigm to dissociate two components of internally guided behavior: Which action to perform (selection component) and when to perform the action (timing component). Our results suggest a neuro-functional dissociation of intentional action timing and intentional action selection. While the RCZ is more strongly activated for the selection component, a part of the superior medial frontal gyrus is more strongly activated for the timing component. However, in a post hoc conducted signal strength analysis we did also observe an interaction between action timing and action selection, indicating that decisional processes concerning action timing and action selection are not completely dissociated but interdependent. Altogether this study challenges the idea of a unitary system supporting voluntary action and instead suggests the existence of different neuroanatomically dissociable subfunctions

Activation of the pre-supplementary motor area but not inferior prefrontal cortex in association with short stop signal reaction time – an intra-subject analysis

Abstract Background Our previous work described the neural processes of motor response inhibition during a stop signal task (SST). Employing the race model, we computed the stop signal reaction time (SSRT) to index individuals' ability in inhibitory control. The pre-supplementary motor area (preSMA), which shows greater activity in individuals with short as compared to those with long SSRT, plays a role in mediating response inhibition. In contrast, the right inferior prefrontal cortex (rIFC) showed greater activity during stop success as compared to stop error. Here we further pursued this functional differentiation of preSMA and rIFC on the basis of an intra-subject approach. Results Of 65 subjects who participated in four sessions of the SST, we identified 30 individuals who showed a difference in SSRT but were identical in other aspects of stop signal performance between the first ("early") and last two ("late") sessions. By comparing regional brain activation between the two sessions, we confirmed greater preSMA but not rIFC activity during short as compared to long SSRT session within individuals. Furthermore, putamen, anterior cerebellum and middle/posterior cingulate cortex also showed greater activity in association with short SSRT. Conclusion These results are consistent with a role of medial prefrontal cortex in controlled action and inferior frontal cortex in orienting attention. We discussed these findings with respect to the process of attentional monitoring and inhibitory motor control during stop signal inhibition.</p

Choosing to inhibit: new insights into the unconscious modulation of free-choices

In our daily activities, we all experience a certain degree of control over our behaviours and the more we feel ‘in control’ the more we are likely to describe our behaviours as self-generated or ‘intentional’. Such intentional control refers to the capacity of humans to perform actions based on internal decisions and motivations, rather than external stimulation. Within the psychological debate on free will, this evidence raised the question on how ‘free-choices’ are taken when decisions are not dictated by immediate external imperatives. The core argument concerns whether voluntary actions follow a conscious intention to act or whether the feeling of being in control is just an epiphenomenon of unconscious neural mechanisms that are the true origin of behaviour. Different components of a free-choice can be isolated and investigated. Participants can choose what action to make, when to make an action, or whether to make an action at all (Brass & Haggard, 2008). Each of these refers to a different aspect of free-choice, but all of them involve the presence of a choice between multiple available options. Studying voluntary responses in this manner and comparing them with action or inhibition in response to a specific external stimulus, allow us to obtain useful insights into the origin of endogenous decisions. Among these components, the decision about whether to act – the so called ‘intentional inhibition’ – has received less attention. Such decision can be taken at almost any stage during motor preparation, until a point of no return (Schultze-Kraft et al., 2016). Libet (1983) controversially suggested that last-moment decisions to inhibit an action involved a purely conscious form of ‘free won’t’ (Libet, Gleason, Wright, & Pearl, 1983). However, alike voluntary actions, conscious decisions to inhibit might also depend on unconscious brain processes. For this reason, to what extent intentional decisions to inhibit are necessarily based on a deliberate choice is still an open question (Parkinson & Haggard, 2014). The present thesis will examine how unperceivable – subliminal – information in the environment, physiological states of the body and ongoing pre-conscious fluctuations in brain activity contribute to generate voluntary decisions to act or to inhibit. Starting from the contemporary debate raging around free will and taking into account the most recent cognitive models of voluntary actions, the introductory section of the thesis will provide an overview on the basic concepts linked to volition (Chapter 1). Particular attention will be given to behavioural inhibition and how this component has been studied along a continuum from ‘stimulus-driven inhibition’ to ‘intentional inhibition’. For each concept introduced, I will provide a review of the current state of the art regarding both the neural and behavioural mechanisms involved. In particular, I shall focus on previous research suggesting that making free-choices activate a specific network of brain activity. Chapter 2 will review current evidence regarding how subliminal information in the environment and psychophysiological states act as modulators for free-choice mechanisms both at the behavioural and neural level. Indeed, there is consistent evidence concerned with the ability of subliminal stimuli to bias our free decisions by influencing the activity within the ‘choice network’. Similarly, psychophysiological states such as the arousal have been shown to moderate a number of cognitive tasks including response inhibition. The second part of the thesis will focus on the empirical work I have conducted to investigate some of the theoretical issues previously introduced. The experiment described in Chapter 3 exploits a ‘Go/Nogo’ paradigm assessing the effect of subliminal priming by highlighting the dramatic effect of congruent and incongruent subliminal information on reaction times and free-choices. As the first experiment validated the paradigm as a meaningful tool to disentangle between forced and free components of making choices in relation to subliminal processing, the functional magnetic resonance (fMRI) experiment described in Chapter 4 capitalizes on the same kind of manipulation. A region of interest (ROI) analysis was conducted to test whether the degree of intentionality of the response and the information provided by subliminal information might modulate the activity within the ‘free-choice network’. In Chapter 5 the effect of an increased level of arousal induced by physical exercise on the performance in the same task will be examined. The experimental section of the present thesis will end with Chapter 6 in which the neural underpinnings of the conscious generation of actions by means of multi-voxel pattern analysis (MVPA) has been investigated. The thesis will end with a general discussion (Chapter 7). Here I shall rely on the evidence presented in the preceding experimental chapters to propose that free-choices are determined by the interplay between brain, body, and sensory environment

Changing your mind before it is too late: the electrophysiological correlates of online error correction during response selection

Inhibiting actions when they are no longer appropriate is essential for adaptive goal-directed behavior. In this study, we used high-density EEG and a standard flanker task to explore the spatiotemporal dynamics of cognitive control and inhibitory mechanisms aimed to prevent the commission of errors. By recording hand-related electromyographic activity, we could disentangle successful from unsuccessful inhibition attempts. Our results confirm that (a) the latency of the error-related negativity (ERN; or Ne) component is too late to be associated with these online inhibitory mechanisms, and (b) instead, a frontal slow negative component with an earlier time course was associated with the implementation of online inhibition. These findings are consistent with single-cell recordings in monkeys showing that the supplementary motor area provides cognitive control signals to the primary motor cortex to exert online inhibition and in turn rectify the course of erroneous actions

The role of the striatum in effort-based decision-making in the absence of reward

Decision-making involves weighing costs against benefits, for instance, in terms of the effort it takes to obtain a reward of a given magnitude. This evaluation process has been linked to the dorsal anterior cingulate cortex (dACC) and the striatum, with activation in these brain structures reflecting the discounting effect of effort on reward. Here, we investigate how cognitive effort influences neural choice processes in the absence of an extrinsic reward. Using functional magnetic resonance imaging in humans, we used an effort-based decision-making task in which participants were required to choose between two options for a subsequent flanker task that differed in the amount of cognitive effort. Cognitive effort was manipulated by varying the proportion of incongruent trials associated with each choice option. Choice-locked activation in the striatum was higher when participants chose voluntarily for the more effortful alternative but displayed the opposite trend on forced-choice trials. The dACC revealed a similar, yet only trend-level significant, activation pattern. Our results imply that activation levels in the striatum reflect a cost-benefit analysis, in which a balance is made between effort discounting and the intrinsic motivation to choose a cognitively challenging task. Moreover, our findings indicate that it matters whether this challenge is voluntarily chosen or externally imposed. As such, the present findings contrast with classical findings on effort discounting that found reductions in striatum activation for higher effort by finding enhancements of the same neural circuits when a cognitively challenging task is voluntarily selected and does not entail the danger of losing reward

Functional correlates of response inhibition in impulse control disorders in Parkinson’s disease

Available online 11 September 2021.Impulse control disorder is a prevalent side-effect of Parkinson’s disease (PD) medication, with a strong negative impact on the quality of life of those affected. Although impulsivity has classically been associated with response inhibition deficits, previous evidence from PD patients with impulse control disorder (ICD) has not revealed behavioral dysfunction in response inhibition. In this study, 18 PD patients with ICD, 17 PD patients without this complication, and 15 healthy controls performed a version of the conditional Stop Signal Task during functional magnetic resonance imaging. Whole-brain contrasts, regions of interest, and functional connectivity analyses were conducted. Our aim was to investigate the neural underpinnings of two aspects of response inhibition: proactive inhibition, inhibition that has been prepared beforehand, and restrained inhibition, inhibition of an invalid inhibitory tendency. We observed that, in respect to the other two groups, PD patients with ICD exhibited hyperactivation of the stopping network bilaterally while performing proactive inhibition. When engaged in restrained inhibition, they showed hyperactivation of the left inferior frontal gyrus, an area linked to action monitoring. Restrained inhibition also resulted in changes to the functional co-activation between inhibitory regions and left inferior parietal cortex and right supramarginal gyrus. Our findings indicate that PD patients with ICD completed the inhibition task correctly, showing altered engagement of inhibitory and attentional areas. During proactive inhibition they showed bilateral hyperactivation of two inhibitory regions, while during restrained inhibition they showed additional involvement of attentional areas responsible for alerting and orienting.This work was supported by grants from the Carlos III Institute of Health (PI11/02109) and the ERA-Neuron program (PIM2010ERN- 0033). Additionally, the authors received the following grants and honoraria: T.E.-P. received a grant from the Spanish Ministry of Economy and Competitiveness (BES-2016-079489). P.M.P.-A. was supported by grants from the Spanish Ministry of Economy and Competitiveness (RYC-2014-15440), the Spanish Ministry of Science and Innovation (PGC2018-093408-B-I00), and the Fundación Tatiana Pérez de Guzmán el Bueno. I.N.-G. was the recipient of a Rio Hortega grant (CM16/00033) from the Carlos III Institute of Health. I.N.-G. received honoraria from Zambon and TEVA for travel and accommodation to attend scientific meetings. M.C.R.-O. received financial support for her research from national and local government institutions in Spain (Carlos III Institute of Health, Basque Country Government, Diputacion Foral Guipuzcoa, and CIBERNED). M.C.R.-O. received honoraria from Zambon, Bial, and Boston Scientific for lectures, travel, and accommodation to attend scientific meetings. BCBL acknowledges support from the Basque Government through the BERC 2018-2021 program