Reduced serotonergic transmission alters sensitivity to cost and reward via 5-HT1A and 5-HT1B receptors in monkeys

PLoS Biol. 2024 Jan 1;22(1):e3002445. doi: 10.1371/journal.pbio.3002445. eCollection 2024 Jan.

Abstract

Serotonin (5-HT) deficiency is a core biological pathology underlying depression and other psychiatric disorders whose key symptoms include decreased motivation. However, the exact role of 5-HT in motivation remains controversial and elusive. Here, we pharmacologically manipulated the 5-HT system in macaque monkeys and quantified the effects on motivation for goal-directed actions in terms of incentives and costs. Reversible inhibition of 5-HT synthesis increased errors and reaction times on goal-directed tasks, indicating reduced motivation. Analysis found incentive-dependent and cost-dependent components of this reduction. To identify the receptor subtypes that mediate cost and incentive, we systemically administered antagonists specific to 4 major 5-HT receptor subtypes: 5-HT1A, 5-HT1B, 5-HT2A, and 5-HT4. Positron emission tomography (PET) visualized the unique distribution of each subtype in limbic brain regions and determined the systemic dosage for antagonists that would achieve approximately 30% occupancy. Only blockade of 5-HT1A decreased motivation through changes in both expected cost and incentive; sensitivity to future workload and time delay to reward increased (cost) and reward value decreased (incentive). Blocking the 5-HT1B receptor also reduced motivation through decreased incentive, although it did not affect expected cost. These results suggest that 5-HT deficiency disrupts 2 processes, the subjective valuation of costs and rewards, via 5-HT1A and 5-HT1B receptors, thus leading to reduced motivation.

MeSH terms

  • Animals
  • Brain / metabolism
  • Carrier Proteins / metabolism
  • Macaca
  • Receptor, Serotonin, 5-HT1B
  • Serotonin Antagonists* / pharmacology
  • Serotonin*

Substances

  • Carrier Proteins
  • Receptor, Serotonin, 5-HT1B
  • Serotonin
  • Serotonin Antagonists

Grants and funding

This work was supported in part by KAKENHI Grants JP22K07339 (to YH), and JP26120733, JP18H04037 and JP20H05955 (to TM) from Japan Society for the Promotion of Science (JSPS), and by the Moonshot Research & Development Program (Millennia Program) from Japan Science and Technology Agency (JST) Grant Number JPMJMS2295 (to TM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.