Patterns of brain activity distinguishing free and forced actions: contribution from sensory cortices

Abstract

The neural basis of decision-making is extremely complex due to the large number of factors that contribute to the outcome of even the most basic actions as well as the range of appropriate responses within many behavioral contexts. To better understand the neural processes underlying basic forms of decision-making, this study utilized an experiment that required a choice about whether to press a button with the right or left hand. These instances of decision-making were compared to identical button presses that were experimentally specified rather than selected by the subject. Magnetoencephalography (MEG) was used to record neural activity during these—what are being termed—free and forced actions and differences in the MEG signal between these two conditions were attributed to the distinct forms of neural activity required to carry out the two types of actions. To produce instances of free and forced behavior, cued button-pressing experiments were performed that use visual, aural, and memorized cues to instruct experimental subjects of the expected outcome of individual trials. Classification analysis of the trials revealed that cortical regions that allowed for the most accurate classification of free and forced actions primarily handle sensory input for the modality used to cue the trials: occipital cortex for visually cued trials, temporal cortex for aurally cued trials, and minor non-localized differences in MEG activity for trials initiated from memory. The differential roles of visual and auditory sensory cortices during free and forced actions provided insight into the neural processing steps that were engaged to initiate cued actions. Specifically, it suggested that detectable differences exist in the activity of sensory cortices and their target sites when subjects performed free and forced actions in response to sensory cues.

State-dependent modulation of positive and negative affective valences by a parabrachial nucleus-to-ventral tegmental area pathway in mice

“…This seemingly contradicting results may attributable to the differential functions of the LPB-VTA pathway based on the behavioral tasks such as the operant conditioning task, which dependents on voluntary behaviors such as self-administration, and the classical conditioning task, which dependents of involuntary behaviors. To support this notion, brain activity that accompanies free and forced actions is different in humans ( Kostelecki et al, 2012 ), suggesting that the same sensory stimulus could lead to different valences when chosen voluntarily versus involuntarily. Intriguingly, Malenka’ groups demonstrated that activation of the amygdala-nigra pathway in mice elicited reinforcement when linked to voluntary actions, but failed to support Pavlovian associations that rely on incentive value signals ( Steinberg et al, 2020 ).…”

Proactive Recruitment of Frontoparietal and Salience Networks for Voluntary Decisions

“…When participants were presented with random monetary gains, Leotti and Delgado ( 2011 ) found that reward circuitry was recruited in anticipation of a voluntary color choice but not preceding a forced choice. Predictive encoding of voluntary decisions has also been evident in areas of the sensory cortex (Kostelecki et al, 2012 ), frontopolar cortex and medial prefrontal cortex (Soon et al, 2008 ) when individuals chose randomly between left or right button presses (Soon et al, 2008 ; Kostelecki et al, 2012 ), or decided whether to add or subtract two numbers (Haynes et al, 2007 ; Soon et al, 2013 ). Furthermore, it was found that frontopolar cortex activity represented the content of simple decisions only if participants had the intention to voluntarily decide between two arbitrary options, but not if they believed themselves to be guessing (Bode et al, 2013 ).…”

Neural dynamics of voluntary decision-making

“…I found that a significant proportion of participants concluded that the pseudorandomised reward stars were not, in fact, random and persisted in strategies they reportedly believed would maximise the number of stars gained. It has commonly been reported in studies with explicitly random outcomes that participants persist in utilising strategies in their choices and will inevitably find patterns in random data where there are none Kostelecki et al, 2012;Lages & Jaworska, 2012;Tricomi et al, 2004;Yu & Cohen, 2008). In our study, the presence of rewarding outcomes may further have contributed to strategic behaviour as participants attempted to respond to perceived micro-variations in the patterns of expected value .…”

“…When participants were presented with random monetary gains, found that reward circuitry was recruited in anticipation of a free colour choice but not preceding a forced choice. Predictive encoding of free decisions has also been evident in areas of the sensory cortex (Kostelecki et al, 2012), frontopolar cortex, and medial prefrontal cortex when individuals chose randomly between left or right button presses (Kostelecki et al, 2012;, or decided whether to add or subtract two numbers . Furthermore, it was found that frontopolar cortex activity represented the content of simple decisions only if participants had the intention to voluntarily decide between two arbitrary options, but not if they believed themselves to be guessing .…”