The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States

Model-based decision-making guides organism behavior by the representation of the relationships between different states. Previous studies have shown that the mammalian hippocampus (Hp) plays a key role in learning the structure of relationships among experiences. However, the hippocampal neural mec...

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Main Authors: Lifang Yang, Fuli Jin, Long Yang, Jiajia Li, Zhihui Li, Mengmeng Li, Zhigang Shang
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:Animals
Subjects:
Online Access:https://www.mdpi.com/2076-2615/14/3/431
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author Lifang Yang
Fuli Jin
Long Yang
Jiajia Li
Zhihui Li
Mengmeng Li
Zhigang Shang
author_facet Lifang Yang
Fuli Jin
Long Yang
Jiajia Li
Zhihui Li
Mengmeng Li
Zhigang Shang
author_sort Lifang Yang
collection DOAJ
description Model-based decision-making guides organism behavior by the representation of the relationships between different states. Previous studies have shown that the mammalian hippocampus (Hp) plays a key role in learning the structure of relationships among experiences. However, the hippocampal neural mechanisms of birds for model-based learning have rarely been reported. Here, we trained six pigeons to perform a two-step task and explore whether their Hp contributes to model-based learning. Behavioral performance and hippocampal multi-channel local field potentials (LFPs) were recorded during the task. We estimated the subjective values using a reinforcement learning model dynamically fitted to the pigeon’s choice of behavior. The results show that the model-based learner can capture the behavioral choices of pigeons well throughout the learning process. Neural analysis indicated that high-frequency (12–100 Hz) power in Hp represented the temporal context states. Moreover, dynamic correlation and decoding results provided further support for the high-frequency dependence of model-based valuations. In addition, we observed a significant increase in hippocampal neural similarity at the low-frequency band (1–12 Hz) for common temporal context states after learning. Overall, our findings suggest that pigeons use model-based inferences to learn multi-step tasks, and multiple LFP frequency bands collaboratively contribute to model-based learning. Specifically, the high-frequency (12–100 Hz) oscillations represent model-based valuations, while the low-frequency (1–12 Hz) neural similarity is influenced by the relationship between temporal context states. These results contribute to our understanding of the neural mechanisms underlying model-based learning and broaden the scope of hippocampal contributions to avian behavior.
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spelling doaj.art-e92f48512da5426d8b9c49e00ae0c3652024-02-09T15:06:39ZengMDPI AGAnimals2076-26152024-01-0114343110.3390/ani14030431The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context StatesLifang Yang0Fuli Jin1Long Yang2Jiajia Li3Zhihui Li4Mengmeng Li5Zhigang Shang6School of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, ChinaSchool of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, ChinaSchool of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, ChinaSchool of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, ChinaSchool of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, ChinaSchool of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, ChinaSchool of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, ChinaModel-based decision-making guides organism behavior by the representation of the relationships between different states. Previous studies have shown that the mammalian hippocampus (Hp) plays a key role in learning the structure of relationships among experiences. However, the hippocampal neural mechanisms of birds for model-based learning have rarely been reported. Here, we trained six pigeons to perform a two-step task and explore whether their Hp contributes to model-based learning. Behavioral performance and hippocampal multi-channel local field potentials (LFPs) were recorded during the task. We estimated the subjective values using a reinforcement learning model dynamically fitted to the pigeon’s choice of behavior. The results show that the model-based learner can capture the behavioral choices of pigeons well throughout the learning process. Neural analysis indicated that high-frequency (12–100 Hz) power in Hp represented the temporal context states. Moreover, dynamic correlation and decoding results provided further support for the high-frequency dependence of model-based valuations. In addition, we observed a significant increase in hippocampal neural similarity at the low-frequency band (1–12 Hz) for common temporal context states after learning. Overall, our findings suggest that pigeons use model-based inferences to learn multi-step tasks, and multiple LFP frequency bands collaboratively contribute to model-based learning. Specifically, the high-frequency (12–100 Hz) oscillations represent model-based valuations, while the low-frequency (1–12 Hz) neural similarity is influenced by the relationship between temporal context states. These results contribute to our understanding of the neural mechanisms underlying model-based learning and broaden the scope of hippocampal contributions to avian behavior.https://www.mdpi.com/2076-2615/14/3/431pigeonhippocampusmodel-based valuationrepresentation of relationshipslocal field potentials
spellingShingle Lifang Yang
Fuli Jin
Long Yang
Jiajia Li
Zhihui Li
Mengmeng Li
Zhigang Shang
The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States
Animals
pigeon
hippocampus
model-based valuation
representation of relationships
local field potentials
title The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States
title_full The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States
title_fullStr The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States
title_full_unstemmed The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States
title_short The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States
title_sort hippocampus in pigeons contributes to the model based valuation and the relationship between temporal context states
topic pigeon
hippocampus
model-based valuation
representation of relationships
local field potentials
url https://www.mdpi.com/2076-2615/14/3/431
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