Environmental complexity modulates information processing and the balance between decision-making systems

Neuron. 2024 Dec 18;112(24):4096-4114.e10. doi: 10.1016/j.neuron.2024.10.004. Epub 2024 Oct 29.

Abstract

Behavior in naturalistic scenarios occurs in diverse environments. Adaptive strategies rely on multiple neural circuits and competing decision systems. However, past studies of rodent decision making have largely measured behavior in simple environments. To fill this gap, we recorded neural ensembles from hippocampus (HC), dorsolateral striatum (DLS), and dorsomedial prefrontal cortex (dmPFC) while rats foraged for food under changing rules in environments with varying topological complexity. Environmental complexity increased behavioral variability, lengthened HC nonlocal sequences, and modulated action caching. We found contrasting representations between DLS and HC, supporting a competition between decision systems. dmPFC activity was indicative of setting this balance, in particular predicting the extent of HC non-local coding. Inactivating mPFC impaired short-term behavioral adaptation and produced long-term deficits in balancing decision systems. Our findings reveal the dynamic nature of decision-making systems and how environmental complexity modulates their engagement with implications for behavior in naturalistic environments.

Keywords: behavior; decision making; dorsolateral striatum; environmental complexity; habit; hippocampus; medial prefrontal cortex; naturalistic environments; place cell; planning; task bracketing.

MeSH terms

  • Animals
  • Corpus Striatum / physiology
  • Decision Making* / physiology
  • Environment*
  • Hippocampus* / physiology
  • Male
  • Prefrontal Cortex* / physiology
  • Rats
  • Rats, Long-Evans*