Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle

PLoS Comput Biol. 2023 Jun 15;19(6):e1011206. doi: 10.1371/journal.pcbi.1011206. eCollection 2023 Jun.

Abstract

Obsessive-compulsive disorder (OCD) has been suggested to be associated with impairment of model-based behavioral control. Meanwhile, recent work suggested shorter memory trace for negative than positive prediction errors (PEs) in OCD. We explored relations between these two suggestions through computational modeling. Based on the properties of cortico-basal ganglia pathways, we modeled human as an agent having a combination of successor representation (SR)-based system that enables model-based-like control and individual representation (IR)-based system that only hosts model-free control, with the two systems potentially learning from positive and negative PEs in different rates. We simulated the agent's behavior in the environmental model used in the recent work that describes potential development of obsession-compulsion cycle. We found that the dual-system agent could develop enhanced obsession-compulsion cycle, similarly to the agent having memory trace imbalance in the recent work, if the SR- and IR-based systems learned mainly from positive and negative PEs, respectively. We then simulated the behavior of such an opponent SR+IR agent in the two-stage decision task, in comparison with the agent having only SR-based control. Fitting of the agents' behavior by the model weighing model-based and model-free control developed in the original two-stage task study resulted in smaller weights of model-based control for the opponent SR+IR agent than for the SR-only agent. These results reconcile the previous suggestions about OCD, i.e., impaired model-based control and memory trace imbalance, raising a novel possibility that opponent learning in model(SR)-based and model-free controllers underlies obsession-compulsion. Our model cannot explain the behavior of OCD patients in punishment, rather than reward, contexts, but it could be resolved if opponent SR+IR learning operates also in the recently revealed non-canonical cortico-basal ganglia-dopamine circuit for threat/aversiveness, rather than reward, reinforcement learning, and the aversive SR + appetitive IR agent could actually develop obsession-compulsion if the environment is modeled differently.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Basal Ganglia*
  • Humans
  • Obsessive Behavior
  • Punishment
  • Reinforcement, Psychology*
  • Reward

Grants and funding

KM was supported by Grant-in-Aid for Scientific Research (No. 20H05049 and 23H03295) of the Ministry of Education, Culture, Sports, Science and Technology in Japan (MEXT) (http://www.mext.go.jp/en/) and the Japan Society for the Promotion of Science (JSPS) (https://www.jsps.go.jp/english/) and the Naito Foundation (https://www.naito-f.or.jp/en/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.