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Expectancy-related changes in firing of dopamine neurons depend on hippocampus

The graphical abstract for this studyFeatured Paper of the Month – January 2025

Published in Nature Communications by Zhewei Zhang,  Yuji Takahashi and Geoffrey Schoenbaum et al. of the NIDA IRP Behavioral Neurophysiology Neuroscience Section.

Summary

The hippocampus (HC) is a brain region that helps us understand our surroundings and predict what might happen next, especially when rewards are involved. It sends information to neurons that release dopamine, a chemical that generates essential “teaching signals” and helps us learn from our experiences.

To understand how this works, we studied rats with hippocampus damage as they played a smell-based game. The game involved four contexts with different reward structures changing over time. What we discovered was fascinating: without a working hippocampus, the rats could only focus on what was happening right now to estimate the current context, instead of using their past experience or prior knowledge.

Thus, we believe that HC provides critical information about the broader context, helping dopamine cells teach our brain not just based on immediate observations but also from past experience. This allows us to learn and make smarter decisions in complex situations.

Publication Information

Zhang, Zhewei; Takahashi, Yuji K; Montesinos-Cartegena, Marlian; Kahnt, Thorsten; Langdon, Angela J; Schoenbaum, Geoffrey

Expectancy-related changes in firing of dopamine neurons depend on hippocampus Journal Article

In: Nat Commun, vol. 15, no. 1, pp. 8911, 2024, ISSN: 2041-1723.

Abstract | Links

@article{pmid39414794,
title = {Expectancy-related changes in firing of dopamine neurons depend on hippocampus},
author = {Zhewei Zhang and Yuji K Takahashi and Marlian Montesinos-Cartegena and Thorsten Kahnt and Angela J Langdon and Geoffrey Schoenbaum},
url = {https://pubmed.ncbi.nlm.nih.gov/39414794/},
doi = {10.1038/s41467-024-53308-z},
issn = {2041-1723},
year = {2024},
date = {2024-10-01},
urldate = {2024-10-01},
journal = {Nat Commun},
volume = {15},
number = {1},
pages = {8911},
abstract = {The orbitofrontal cortex (OFC) and hippocampus (HC) both contribute to the cognitive maps that support flexible behavior. Previously, we used the dopamine neurons to measure the functional role of OFC. We recorded midbrain dopamine neurons as rats performed an odor-based choice task, in which expected rewards were manipulated across blocks. We found that ipsilateral OFC lesions degraded dopaminergic prediction errors, consistent with reduced resolution of the task states. Here we have repeated this experiment in male rats with ipsilateral HC lesions. The results show HC also shapes the task states, however unlike OFC, which provides information local to the trial, the HC is necessary for estimating upper-level hidden states that distinguish blocks. The results contrast the roles of the OFC and HC in cognitive mapping and suggest that the dopamine neurons access rich information from distributed regions regarding the environment's structure, potentially enabling this teaching signal to support complex behaviors.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The orbitofrontal cortex (OFC) and hippocampus (HC) both contribute to the cognitive maps that support flexible behavior. Previously, we used the dopamine neurons to measure the functional role of OFC. We recorded midbrain dopamine neurons as rats performed an odor-based choice task, in which expected rewards were manipulated across blocks. We found that ipsilateral OFC lesions degraded dopaminergic prediction errors, consistent with reduced resolution of the task states. Here we have repeated this experiment in male rats with ipsilateral HC lesions. The results show HC also shapes the task states, however unlike OFC, which provides information local to the trial, the HC is necessary for estimating upper-level hidden states that distinguish blocks. The results contrast the roles of the OFC and HC in cognitive mapping and suggest that the dopamine neurons access rich information from distributed regions regarding the environment's structure, potentially enabling this teaching signal to support complex behaviors.

Close

  • https://pubmed.ncbi.nlm.nih.gov/39414794/
  • doi:10.1038/s41467-024-53308-z

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