Characterizing habit learning in the human brain at the individual and group levels: a multi-modal MRI study

Abstract

The dual-process theory of action control postulates that there are two competitive and complementary mechanisms that control our behavior: a goal-directed system that executes deliberate actions, explicitly aimed toward a particular outcome, and a habitual system that autonomously execute well-learned actions, typically following an encounter with a previously associated cue. In line with dual-process theory, animal studies have provided convincing evidence for dissociable neural mechanisms, mainly manifested in cortico-striatal regions, involved in goal-directed and habitual action control. While substantial progress has been made in characterizing the neural mechanism underlying habit learning in animals, we still lack knowledge on how habits are formed and maintained in the human brain. Thus far only one study, conducted more than a decade ago by Tricomi et al. (2009), has been able to induce habitual behavior in humans via extensive training. This study also implicated the posterior putamen in the process, using functional magnetic resonance imaging (fMRI). However, recent attempts to replicate the behavioral results of this study were not successful. This leaves the research of human habits, and particularly the research of their formation through extensive repetition, as well as their neural basis, limited and far behind the animal research in the field. This motivated us to (1) attempt to replicate the behavioral and imaging main findings of Tricomi et al., (2) identify further functional and microstructural neural modifications associated with habit formation and manifestation, and (3) investigate the relationships between functional and structural plasticity and individual differences in habit expression. To this end, in this registered report we used Tricomi et al.'s free-operant task along with multi-modal MRI methods in a well-powered sample (n=123). In this task participants' sensitivity to outcome devaluation (an index of goal-directed/habitual action control) is tested following either short or extensive training. In contrast to our hypothesis, we were not able to demonstrate habit formation as a function of training duration nor were we able to relate any functional or microstructural plasticity in the putamen with individual habit expression. We found that a pattern of increased activations in the left head of caudate that re-occurred across each day's training is associated with goal directed behavior and that increased processing of devalued cues in low-level visual regions was indicative of goal-directed behavior (and vice versa). In a follow-up exploratory analysis comparing habitual and goal-directed subgroups within each experimental group, we found that elevated activations in frontoparietal regions during early stages of training, as well as increased reactivity towards still-valued cues in somatosensory and superior parietal regions were found in individuals that were more inclined to perform goal-directed behavior (compared with more habitual individuals). Taken together, regions commonly implicated in goal-directed behavior were most predictive of individual habit expression. Finally, we also found that differential patterns of training-related microstructural plasticity, as measured with diffusion MRI, in midbrain dopaminergic regions were associated with habit expression. This work provides new insights into the neural dynamics involved in individual habit formation/expression and encourages the development and testing of new, more sensitive, procedures for experimental habit induction in humans.

A novel free-operant framework enables experimental habit induction in humans

“…This joins our general proposition that the expression of habits, especially when they are no longer adaptive, is a subtle effect and its stability is subject to a variety of factors. The observation that a subset of participants in the extensive training groups manifested sensitivity to outcome devaluation (which is in line with previous evidence 25,31,32 ) perhaps indicates that habit formation is not a unitary deterministic process. We therefore propose that acquiring large datasets is of great value to further establish the effects found here and explore other factors implicated in habit learning.…”

“…Experimental habit induction in humans has constituted a significant hurdle for researchers in the field. Promising results of habit formation following extensive training were demonstrated in one study 30 (indexed by insensitivity to outcome devaluation), but a series of attempts were not successful in replicate those findings 25,31,32 . Other attempts targeting decreased sensitivity to outcome Fig.…”

“…The importance of this translational aspect is emphasized by findings showing that training animals on more than one instrumental associative structure have not led to habit formation [42][43][44] . It is possible that the presence of two similar associative structures in a similar general context encourages goal-directed control in the presence of choices between actions (discussed in 45 ) or short trials 31 and enhances habit expression in free-operant settings due to generalization of training on similar associative structures 25,31,32 . If this is indeed the case, avoiding the use of more than one associative structure may be the key to successful experimental habit induction; (3) We trained participants on an action sequence rather than on a single action.…”

“…Only a single study successfully demonstrated the shift in action control as a function of training duration 30 . However, those results have not been replicated thus far and have been challenged in multiple replication attempts 25,31,32 . Therefore, to date, the research of habit formation in humans has been left behind its animal counterpart, which impedes our ability to understand the mechanisms underlying habit formation and the development of potential interventions.…”

A novel free-operant framework enables experimental habit induction in humans

“…However, perhaps the most basic demonstration of habit formation through prolonged training has yet to be reliably demonstrated. Only a single study has successfully demonstrated the shift in action control as a function of training duration (Tricomi et al, 2009 ) but those results have not been replicated thus far and have been challenged in multiple replication attempts (de Wit et al, 2018 ; Gera et al, 2022 ; Pool et al, 2022 ). This impedes our ability to understand the mechanisms underlying habit formation and the development of potential interventions, and has left the research of habit formation in humans far behind its animal counterpart.…”