Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigms

The IntelliCage allows automated testing of cognitive abilities of mice in a social home cage environment without handling by human experimenters. Restricted water access in combination with protocols in which only correct responses give access to water is a reliable learning motivator for hippocamp...

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Main Authors: Xueqian Ma, Beatrice Schildknecht, Adrian C. Steiner, Irmgard Amrein, Martina Nigri, Giulia Bramati, David P. Wolfer
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Behavioral Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnbeh.2023.1232546/full
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author Xueqian Ma
Beatrice Schildknecht
Adrian C. Steiner
Irmgard Amrein
Irmgard Amrein
Martina Nigri
Giulia Bramati
David P. Wolfer
David P. Wolfer
author_facet Xueqian Ma
Beatrice Schildknecht
Adrian C. Steiner
Irmgard Amrein
Irmgard Amrein
Martina Nigri
Giulia Bramati
David P. Wolfer
David P. Wolfer
author_sort Xueqian Ma
collection DOAJ
description The IntelliCage allows automated testing of cognitive abilities of mice in a social home cage environment without handling by human experimenters. Restricted water access in combination with protocols in which only correct responses give access to water is a reliable learning motivator for hippocampus-dependent tasks assessing spatial memory and executive function. However, water restriction may negatively impact on animal welfare, especially in poor learners. To better comply with the 3R principles, we previously tested protocols in which water was freely available but additional access to sweetened water could be obtained by learning a task rule. While this purely appetitive motivation worked for simple tasks, too many mice lost interest in the sweet reward during more difficult hippocampus-dependent tasks. In the present study, we tested a battery of increasingly difficult spatial tasks in which water was still available without learning the task rule, but rendered less attractive either by adding bitter tasting quinine or by increasing the amount of work to obtain it. As in previous protocols, learning of the task rule provided access to water sweetened with saccharin. The two approaches of dual motivation were tested in two cohorts of female C57BL/6 N mice. Compared to purely appetitive motivation, both novel protocols strongly improved task engagement and increased task performance. Importantly, neither of the added disincentives had an adverse impact on liquid consumption, health status or body weight of the animals. Our results show that it is possible to refine test protocols in the IntelliCage so that they challenge cognitive functions without restricting access to water.
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spelling doaj.art-68f6431fa5f447198971897a5e9d406c2023-11-16T17:43:23ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532023-11-011710.3389/fnbeh.2023.12325461232546Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigmsXueqian Ma0Beatrice Schildknecht1Adrian C. Steiner2Irmgard Amrein3Irmgard Amrein4Martina Nigri5Giulia Bramati6David P. Wolfer7David P. Wolfer8Department of Health Sciences and Technology, Institute of Human Movement Sciences and Sport, ETH, Zürich, SwitzerlandDepartment of Health Sciences and Technology, Institute of Human Movement Sciences and Sport, ETH, Zürich, SwitzerlandFaculty of Medicine, Institute of Anatomy, University of Zürich, Zürich, SwitzerlandDepartment of Health Sciences and Technology, Institute of Human Movement Sciences and Sport, ETH, Zürich, SwitzerlandFaculty of Medicine, Institute of Anatomy, University of Zürich, Zürich, SwitzerlandDepartment of Health Sciences and Technology, Institute of Human Movement Sciences and Sport, ETH, Zürich, SwitzerlandDepartment of Health Sciences and Technology, Institute of Human Movement Sciences and Sport, ETH, Zürich, SwitzerlandDepartment of Health Sciences and Technology, Institute of Human Movement Sciences and Sport, ETH, Zürich, SwitzerlandFaculty of Medicine, Institute of Anatomy, University of Zürich, Zürich, SwitzerlandThe IntelliCage allows automated testing of cognitive abilities of mice in a social home cage environment without handling by human experimenters. Restricted water access in combination with protocols in which only correct responses give access to water is a reliable learning motivator for hippocampus-dependent tasks assessing spatial memory and executive function. However, water restriction may negatively impact on animal welfare, especially in poor learners. To better comply with the 3R principles, we previously tested protocols in which water was freely available but additional access to sweetened water could be obtained by learning a task rule. While this purely appetitive motivation worked for simple tasks, too many mice lost interest in the sweet reward during more difficult hippocampus-dependent tasks. In the present study, we tested a battery of increasingly difficult spatial tasks in which water was still available without learning the task rule, but rendered less attractive either by adding bitter tasting quinine or by increasing the amount of work to obtain it. As in previous protocols, learning of the task rule provided access to water sweetened with saccharin. The two approaches of dual motivation were tested in two cohorts of female C57BL/6 N mice. Compared to purely appetitive motivation, both novel protocols strongly improved task engagement and increased task performance. Importantly, neither of the added disincentives had an adverse impact on liquid consumption, health status or body weight of the animals. Our results show that it is possible to refine test protocols in the IntelliCage so that they challenge cognitive functions without restricting access to water.https://www.frontiersin.org/articles/10.3389/fnbeh.2023.1232546/fullhome cage monitoringincentive learningdisincentive learningappetitive learningaversive learninganimal welfare
spellingShingle Xueqian Ma
Beatrice Schildknecht
Adrian C. Steiner
Irmgard Amrein
Irmgard Amrein
Martina Nigri
Giulia Bramati
David P. Wolfer
David P. Wolfer
Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigms
Frontiers in Behavioral Neuroscience
home cage monitoring
incentive learning
disincentive learning
appetitive learning
aversive learning
animal welfare
title Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigms
title_full Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigms
title_fullStr Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigms
title_full_unstemmed Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigms
title_short Refinement of IntelliCage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive-disincentive paradigms
title_sort refinement of intellicage protocols for complex cognitive tasks through replacement of drinking restrictions by incentive disincentive paradigms
topic home cage monitoring
incentive learning
disincentive learning
appetitive learning
aversive learning
animal welfare
url https://www.frontiersin.org/articles/10.3389/fnbeh.2023.1232546/full
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