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Handbook of Object Novelty Recognition
Handbook of Object Novelty Recognition
Handbook of Object Novelty Recognition
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Handbook of Object Novelty Recognition

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Handbook of Object Novelty Recognition, Volume 26, synthesizes the empirical and theoretical advances in the field of object recognition and memory that have occurred since the development of the spontaneous object recognition task. The book is divided into four sections, covering vision and perception of object features and attributions, definitions of concepts that are associated with object recognition, the influence of brain lesions and drugs on various memory functions and processes, and models of neuropsychiatric disorders based on spontaneous object recognition tasks. A final section covers genetic and developmental studies and gender and hormone studies.

  • Details the brain structures and the neural circuits that underlie memory of objects, including vision and olfaction
  • Provides a thorough description of the object novelty recognition task, variations on the basic task, and methods and techniques to help researchers avoid common pitfalls
  • Assists researchers in understanding all aspects of object memory, conducting object novelty recognition tests, and producing reliable, reproducible results
LanguageEnglish
Release dateNov 16, 2018
ISBN9780128120149
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    Handbook of Object Novelty Recognition - Academic Press

    Handbook Of Object Novelty Recognition

    Editors

    Abdel Ennaceur

    Maria Angelica de Souza Silva

    Table of Contents

    Cover image

    Title page

    Copyright

    Contributors

    Preface

    Chapter 1. Object Novelty Recognition Memory

    1. Introduction

    2. Object Novelty Recognition Memory Test Uses

    3. Diversity and Exploitation of Test Parameters

    4. Plurality and Ambiguity of the Object Novelty Recognition Memory Test Identifiers

    5. Object Recognition and Working Memory

    6. Object Novelty Recognition Memory Test and Variants

    7. Open Field and Mazes

    8. Object Features

    9. Simple Versus Complex Objects Versus Similarity

    10. Single Object and Different Object in the Sample Phase

    11. Locomotor Activity, Exploration and Memory

    12. Pretest Habituation

    13. Measurements and Analysis

    14. Conclusion

    Chapter 2. Theories and Concepts

    1. Introduction

    2. Neuroanatomy of the Medial Temporal Lobe

    3. Theories of Hippocampal Memory Function

    4. Familiarity and Recollection

    5. Object Perception and Recognition

    6. Spatial Perception and Recognition

    7. Temporal Perception and Recognition

    8. Towards a Unifying Model of Recognition and Recall

    9. Conclusions

    Chapter 3. Object Novelty Memory Tests: Methods, Test Procedures and Measurements

    1. Object Novelty Recognition

    2. Object Location Recognition

    3. Object in Place Recognition

    4. Object in Context Recognition

    5. Object Temporal Order Recognition

    6. Object Pattern Separation

    7. Conclusions

    Chapter 4. The Mouse Visual System and Visual Perception

    1. Historical Perspective

    2. Overview of central visual pathways

    3. Eyes and Retina

    4. Superior Colliculus

    5. The First-Order Visual Thalamic Relay: dLGN

    6. Primary Visual Cortex and Higher Visual Areas

    7. Role of Visual Cortex

    8. Top-Down Connections to Mouse V1

    Chapter 5. Methodological Approaches to the Behavioural Investigation of Visual Perception in Rodents

    1. Introduction

    2. Approaches Based on Collection of Spontaneous Responses

    3. Approaches Based on Explicitly Training Rodents in Visual Discrimination Tasks

    4. Advanced Psychophysical Procedures

    Chapter 6. Exploiting Novelty and Oddity Exploratory Preferences in Rodents to Study Multisensory Object Memory and Perception

    1. Introduction

    2. Development of Multisensory Object Processing Tasks for Rodents

    3. Neurobiology of Rodent Crossmodal Object Recognition

    4. Clinical Relevance of Rodent Multisensory Object Processing Tasks

    5. Conclusions

    Chapter 7. Variants of the Spontaneous Recognition Procedure Assessing Multisensory Integration Reveal Behavioral Alterations in Rodent Models of Psychiatric and Neurological Disorders

    1. Introduction

    2. Multisensory Integration in Psychiatric Disorders

    3. Rodent Tasks

    4. Multisensory Integration Object Recognition Deficits in Rodent Models of Psychiatric and Neurological Disorders

    5. Conclusions and Future Directions

    Chapter 8. Visual Object Recognition Task: A Translational Paradigm to Evaluate Sustained Attention Across Species

    1. Introduction

    2. From Novel Object Recognition to Virtual Object Recognition Task

    3. Conclusions

    Glossary

    Chapter 9. Object Novelty and Object Location Recognition Memory in Fish – Recent Advances

    1. Introduction

    2. Novel Object Recognition Testing in Fish

    3. Episodic-Like Memory Testing in Fish

    4. Conclusion

    Chapter 10. Integration of Human Eye-Tracking Responses and Object Recognition Test Performance

    1. Introduction

    2. The Novel Image Novel Location Test

    3. Use of the NINL Test and Comparison of NINL Test Performance in Humans With That of Object Recognition in Mice

    4. Integration of Eye-Tracking and NINL Test Performance

    5. Relationship Between Integration of Eye-Tracking Response and NINL Performance Measures to Performance on the Raven's Fluid Intelligence Test

    6. Conclusions

    Chapter 11. Developmental Trajectories of Object and Spatial Recognition Memory in Infant Rhesus Macaques

    1. Introduction

    2. An Early Developing Object Recognition System

    3. Protracted Maturation of Spatial Recognition Memory

    4. Relationships to Human Memory Development

    Chapter 12. Perirhinal Cortex Lesions and Spontaneous Object Recognition Memory in Rats: Detecting Novelty But Not Distinguishing Novelty

    1. Introduction

    2. Spontaneous Object Recognition Memory and the Perirhinal Cortex

    3. Issues of Exploration and Habituation

    4. The Level of Exploration Paradox

    5. The Bow-Tie Maze

    6. The Bow-Tie Maze, Perirhinal Cortex Lesions, Levels of Exploration, and Habituation

    7. The Bow-Tie Maze, Perirhinal Cortex Lesions, and Interference

    8. Novelty Discrimination Versus Novelty Detection

    9. Future Directions

    Chapter 13. Using the Spontaneous Object Recognition Memory Tasks to Uncover the Neural Circuitry of Recognition Memory: The Importance of Thalamic Nuclei

    1. Introduction

    2. Thalamus and Recognition Memory

    3. The Effect of Damage in the Thalamus to Recognition Memory in the Rat

    4. Conclusions

    Chapter 14. The Hippocampal-Cortical Networks Subserving Episodic Memory and Its Component Memory Systems for Object, Place and Temporal Order

    1. Behavioural Paradigms for Measuring Object-, Place-, Temporal- and Episodic-Memory Based on Object Exploration

    2. The Prefrontal Cortex, Entorhinal Cortex and Hippocampus as a Memory System

    3. The Role of the Prefrontal Cortex

    4. The Role of the Entorhinal Cortex

    5. The Role of the Hippocampus

    6. The Functional Hippocampal-Cortical Network of Episodic Memory

    Chapter 15. The Papez Circuit and Recognition Memory: Contributions of the Medial Diencephalon and Retrosplenial Cortex to What, Where and When Aspects of Object Recognition Memory

    1. Introduction

    2. Anatomical Considerations

    3. The Mammillary Bodies and Mammillothalamic Tract

    4. Anterior Thalamic Nuclei

    5. Retrosplenial Cortex

    6. Conclusions

    Chapter 16. Correlates of Object Exploration and Recognition Memory in Mouse Anterior Cingulate Cortex

    1. Introduction

    2. Background

    3. Experimental Design

    4. Correlates in the Caudal Anterior Cingulate Cortex

    5. Interpreting the Data

    6. Summary

    Chapter 17. The Amygdala and Emotional Arousal Effects on Object Recognition Memory

    1. Introduction

    2. Stress Hormone Effects on Object Recognition Memory

    3. Role of the Amygdala

    4. Amygdala Interactions With Other Brain Regions

    5. Conclusions

    Chapter 18. Immediate-Early Gene Expression in Neural Circuits Related to Object Recognition Memory

    1. Introduction

    2. Novel Object Recognition Tests

    3. Immediate-Early Genes

    4. Immediate-Early Genes and Object Recognition Tests

    5. Limitations and Future Directions

    6. Conclusion

    Chapter 19. Item-Place Encoding Through Hippocampal Long-Term Depression

    1. Introduction

    2. Hippocampal LTP Selects and Associates Synaptic Networks to Support and Extend Memory Encoding

    3. Hippocampal LTD Supports the Inclusion of Content Detail to Spatial Representations and Promotes Differentiation of Similar Representations

    4. Microscale and Macroscale Object-Place Learning Are Processed by Different Neuronal Subcompartments Within the Hippocampus

    5. Contribution of Neurotransmitter Receptors and Signal Cascades to Encoding of Item-Place Experience Through LTD

    6. Conclusions

    Chapter 20. The Contribution of Recollection, Familiarity and Discrimination to Object Recognition Deficits in Advanced Age

    1. Introduction

    2. Assessing Object Recognition in Older Adults

    3. Assessing Object Recognition in Animal Models of Ageing

    4. Conclusions

    Chapter 21. The Value of the Object Recognition Paradigm in Investigating Animal Models of Alzheimer's Disease: Advances and Future Directions

    1. Introduction

    2. Neuropathology and Object Recognition Memory in Alzheimer's Disease

    3. Object Recognition Paradigms Used in Humans

    4. Object Exploration Paradigm Used in Animal Models of AD

    5. Neuroanatomical Substrates of Object Recognition and Object Location Tasks

    6. Recognition Memory and AD-Like Pathology in Animal Models

    7. Conclusions

    Chapter 22. Mild Traumatic Brain Injuries and Object Recognition

    1. Introduction

    2. Novel Object Recognition as a Means of Assessing mTBI

    3. Weight Drop Model

    4. Fluid Percussion Injury Model

    5. Controlled Cortical Impact Model

    6. Open Air Blast Traumatic Brain Injury Model

    7. Conclusion

    Chapter 23. The Use of Object Recognition Task in Animal Models of Attention-Deficit Hyperactivity Disorder

    1. Introduction

    2. The Use of Laboratory Rodents in ADHD Research

    3. Candidate Genes for the Study of ADHD

    4. Studies Using Object Recognition Task in Animal Models of ADHD

    5. Conclusions

    Chapter 24. The Neuropharmacology of What, Where, When: How Dopamine Modulates Recognition Memory for Objects and Their Contexts

    1. DA Depletion Dissociates What, Where and When

    2. Drug Studies to Distinguish the Encoding, Consolidation and Retrieval of What and Where

    3. Pharmacogenetic Approaches: DA and the Synaptic Plasticity Underlying OR

    4. Behavioural Analyses: Memory Mechanisms of OR

    5. Conclusions

    Chapter 25. The Role of Cholinergic System in Novel Object Recognition

    List of Abbreviations

    1. Introduction

    2. Novel Object Recognition and the Brain Cholinergic System

    3. Administration of Muscarinic Antagonists

    4. Administration of Nicotinic Antagonists

    5. Effect of Lesions of the Cholinergic System and of Intracerebral Amyloid Peptide (Aβ) Injections

    6. The Cholinergic System and NOR Performance in Old Rats

    7. Drugs Stimulating the Cholinergic System Restore NOR performance

    8. Conclusions

    Chapter 26. Nicotinic Receptor Ligands and Novel Object Recognition

    1. Introduction

    2. The Novel Object Recognition Test Procedure

    3. Nicotinic Acetylcholine Receptor Effects on Novel Object Recognition Memory

    4. Conclusion

    Chapter 27. Novel Object Recognition Test in Rodents:: Which Roles for Serotonin Receptors?

    1. Introduction

    2. Pharmacological Modulation of 5-HTRs by Systemic Administration on Novel Object Recognition Performances: Encoding, Consolidation and Retrieval

    3. Pharmacological Modulation of 5-HTR by Local Administration and Novel Object Recognition Performances

    4. Chronic Modulation of 5-HTR and Novel Object Recognition Performances

    5. Conclusion

    Chapter 28. Object Recognition and Object Location Recognition Memory – The Role of Dopamine and Noradrenaline

    1. Introduction

    2. Object Recognition and Object Location Memory

    3. Catecholamines in Alzheimer's Disease

    Chapter 29. Histaminergic Modulation of Recognition Memory

    1. Introduction

    2. Central Histaminergic System

    3. Histamine Receptors

    4. Histamine Functions in the CNS

    5. Role of Histamine and Its Receptors on Recognition Memory

    6. The Histaminergic System as a Therapeutic Target for the Treatment of Cognitive Impairment Associated With Neuropsychiatric Disorders: Challenges and Opportunities

    7. Concluding Remarks

    Chapter 30. The Roles of Neurotrophins in Novel Object Recognition

    1. Introduction

    2. Mechanisms Underlying Novel Object Recognition

    3. Neurotrophins

    4. Brain-Derived Neurotrophic Factor and Recognition Memory in Humans

    5. Conclusions

    Chapter 31. Cannabinoid Modulation of Object Recognition and Location Memory—A Preclinical Assessment

    1. Introduction

    2. Preclinical Assessment of Object Recognition Memory: Novel Object Recognition and Novel Object Location Tests

    3. Acute Effects of Cannabinoids on NOR and NOL Memory

    4. Effects of Chronic Cannabinoid Treatment on NOR and NOL Memory

    5. Effects of Cannabinoid Receptor 1 Gene Modification on NOR and NOL Memory

    6. Molecular Mechanisms Underlying Cannabinoid-Induced Changes to NOR and NOL Memory in Control Animals

    7. The eCB System as a Treatment Target to Reverse Cognitive Impairment

    8. Conclusions

    Chapter 32. Hormonal Regulation of Object Memory Consolidation

    1. Object Recognition and Object Placement: An Overview

    2. Hippocampal Involvement in Object Learning and Memory

    3. Additional Brain Regions Involved in Object Learning

    4. Oestrogens and Object Learning

    5. Conclusions and Future Directions

    Chapter 33. The Role of Sex and Sex Steroids in the Novel Object Recognition Task

    1. Introduction

    2. Ovarian Steroids

    3. Novel Object Recognition Task

    4. Sex Differences

    5. Endogenous Ovarian Steroids

    6. Exogenous Ovarian Steroids

    7. Limitations and Implications

    8. Conclusions

    Chapter 34. Sex Differences in Cognitive Responses to Stress in Rodents

    1. Introduction

    2. Background Information About Recognition Memory Testing

    3. Stress Impairs Recognition Memory in Male but Not Female Rats

    4. Influence of Psychological and Performance Parameters on Memory

    5. Neural Effects of Stress

    6. Sex Differences in the Stress Response in Relation to Mental Health

    7. Conclusions

    Chapter 35. Glutamate Signalling in Object Novelty Recognition Memory Tests

    1. Introduction

    2. Glutamate Signalling

    3. Conclusions

    Chapter 36. The Role of Ketamine in Object Recognition Memory in Rodents

    1. Introduction

    2. Ketamine and Object Recognition Memory

    3. Mechanism of Action of Ketamine on Memory

    4. Conclusions

    Chapter 37. Nitrinergic Signalling in Object Novelty Recognition

    1. Introduction

    2. Nitric Oxide Signalling

    3. Conclusions

    Chapter 38. Phosphodiesterase Inhibitors in Object Recognition and Object Location Memory Tests

    1. Introduction

    2. The Role of Phosphodiesterases in Signal Transduction

    3. Phosphodiesterases and Memory

    4. Phosphodiesterase Inhibitors in the Object Recognition Test and Object Location Test

    5. Conclusion

    Index

    Copyright

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    Contributors

    John P. Aggleton     School of Psychology, Cardiff University, Cardiff, United Kingdom

    Elentina K. Argyrousi     Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, Maastricht, MD, The Netherlands

    Jocelyne Bachevalier     Yerkes National Primate Research Center and Department of Psychology, Emory University, Atlanta, GA, United States

    Nadir M. Balba     Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United States

    F.F. Barbosa     Memory and Cognition Studies Laboratory, Department of Psychology, Universidade Federal da Paraíba, João Pessoa, Brazil

    Carol A. Barnes

    Evelyn F. McKnight Brain Institute, University of Florida, Gainesville, FL, United States

    Division of Neural Systems Memory and Aging, University of Arizona, Tucson, AZ, United States

    Departments of Psychology, University of Arizona, Tucson, AZ, United States

    Neurology and Neuroscience, University of Arizona, Tucson, AZ, United States

    Areg Barsegyan

    Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The Netherlands

    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands

    Federico Bermudez-Rattoni     División de Neurociencias, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México, Mexico

    Arjan Blokland     Department of Neuropsychology and Psychopharmacology, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, MD, The Netherlands

    Valentine Bouet     Normandie Univ., UNICAEN, INSERM, COMETE, Caen, France

    Michel Boulouard     Normandie Univ., UNICAEN, INSERM, COMETE, Caen, France

    Rachel Bowman     Department of Psychology, Sacred Heart University, Fairfield, CT, United States

    Daniela Braida     Department of Medical Biotechnology and Translational Medicine, Università degli Studi di Milano, Milan, Italy

    Sara N. Burke

    McKnight Brain Institute, Department of Neuroscience, University of Florida, Gainesville, FL, United States

    Institute on Aging, University of Florida, Gainesville, FL, United States

    Laura Busse

    Division of Neurobiology, Department Biology II, LMU Munich, Munich, Germany

    Bernstein Center for Computational Neuroscience, LMU Munich, Munich, Germany

    Patrick M. Callahan

    Department of Pharmacology and Toxicology, Medical College of Georgia, Augusta University, Augusta, GA, United States

    Small Animal Behavior Core, Augusta University, Augusta, GA, United States

    H.J. Cassaday     School of Psychology, The University of Nottingham, Nottingham, United Kingdom

    Owen Y. Chao     Department of Biomedical Sciences, School of Medicine, University of Minnesota, Duluth MN, United States

    Yanfen Chen

    Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The Netherlands

    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands

    Rose Chesworth     School of Medicine, Western Sydney University, Campbelltown, NSW, Australia

    Alessia Costa     Department of Neuroscience, Psychology, Drug Research and Child Health, Section of Pharmacology and Toxicology, University of Florence, Florence, Italy

    Samantha D. Creighton

    Department of Psychology, University of Guelph, Guelph, ON, Canada

    Collaborative Neuroscience Program, University of Guelph, Guelph, ON, Canada

    Maria A. de Souza Silva     Center for Behavioral Neuroscience, Institute of Experimental Psychology, Heinrich-Heine University Düsseldorf, Düsseldorf, Germany

    Alessandro Di Filippo     Visual Neuroscience Lab, International School for Advanced Studies (SISSA), Trieste, Italy

    Abdel Ennaceur     Department of Pharmacy, University of Sunderland, Sunderland, United Kingdom

    Angela Patricia França

    Department of Pharmacology, Center of Biological Sciences, Universidade Federal de Santa Catarina (UFSC), Campus Trindade, Florianópolis, Brazil

    Graduate Program of Neuroscience, Center of Biological Science, Universidade Federal de Santa Catarina (UFSC), Campus Trindade, Florianópolis, Brazil

    Thomas Freret     Normandie Univ., UNICAEN, INSERM, COMETE, Caen, France

    Karyn M. Frick     Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, WI, United States

    Maria Grazia Giovannini     Department of Health Sciences, Section of Clinical Pharmacology and Oncology, University of Florence, Florence, Italy

    Sandra Glazer

    Department of Anatomy and Anthropology, Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Department of Psychology, Miami University, Oxford, OH, United States

    Andrea Gogos     Hormones in Psychiatry Laboratory, The Florey Institute of Neuroscience and Mental Health, Parkville VIC, Australia

    Kioko Guzman-Ramos     Departamento de Ciencias de la Salud, División de Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana Unidad Lerma, México, Mexico

    Trevor J. Hamilton

    Department Psychology, MacEwan University, Edmonton, AB, Canada

    Neuroscience and Mental Health Institute, University of Alberta, AB, Canada

    Pim R.A. Heckman     Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, Maastricht, MD, The Netherlands

    John G. Howland     Department of Physiology, University of Saskatchewan, Saskatoon, SK, Canada

    Joseph P. Huston     Center for Behavioral Neuroscience, Institute of Experimental Psychology, Heinrich-Heine University Düsseldorf, Düsseldorf, Germany

    Geison Souza Izídio

    Department of Pharmacology, Center of Biological Sciences, Universidade Federal de Santa Catarina (UFSC), Campus Trindade, Florianópolis, Brazil

    Laboratory of Behavioral Genetics, Department of Cellular Biology, Embryology and Genetics, Universidade Federal de Santa Catarina (UFSC), Florianópolis, Brazil

    Tim Karl

    School of Medicine, Western Sydney University, Campbelltown, NSW, Australia

    Neuroscience Research Australia, Randwick, NSW, Australia

    Áine Kelly     Department of Physiology, School of Medicine, & Trinity College Institute of Neuroscience & Trinity Biomedical Sciences Institute, Trinity College Dublin, University of Dublin, Dublin, Ireland

    Snezana Kusljic

    Hormones in Psychiatry Laboratory, The Florey Institute of Neuroscience and Mental Health, Parkville VIC, Australia

    Department of Nursing, University of Melbourne, Parkville, VIC, Australia

    Garet P. Lahvis     Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United States

    Victoria Luine     Department of Psychology, Hunter College of CUNY, New York, NY, United States

    Denise Manahan-Vaughan     Ruhr University Bochum, Medical Faculty, Department of Neurophysiology, Bochum, Germany

    Wendie N. Marks     Department of Physiology, University of Saskatchewan, Saskatoon, SK, Canada

    Chantal Mathis     Université de Strasbourg, CNRS, UMR 7364, Laboratoire de Neurosciences Cognitives et Adaptatives (LNCA), Strasbourg, France

    Madeleine McCarthy     Hormones in Psychiatry Laboratory, The Florey Institute of Neuroscience and Mental Health, Parkville VIC, Australia

    Krista A. Mitchnick

    Department of Psychology, University of Guelph, Guelph, ON, Canada

    Collaborative Neuroscience Program, University of Guelph, Guelph, ON, Canada

    Perla Moreno-Castilla     División de Neurociencias, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México, Mexico

    Andrew J.D. Nelson     School of Psychology, Cardiff University, Cardiff, United Kingdom

    Dean Paes     Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, Maastricht, MD, The Netherlands

    Daniel Palmer     Department of Physiology & Pharmacology, Robarts Research Institute, Western University, London, ON, Canada

    Madeline E. Parker     Department of Physiology, University of Saskatchewan, Saskatoon, SK, Canada

    Maria Beatrice Passani     Department of Health Sciences, Section of Clinical Pharmacology and Oncology, University of Florence, Florence, Italy

    Giancarlo Pepeu     Department of Neurosciences, Psychology, Drug Research and Child Health (NEUROFARBA), Section of Pharmacology and Toxicology, University of Florence, Florence, Italy

    James C. Perry     School of Psychology, Cardiff University, Cardiff, United Kingdom

    Chaim G. Pick

    Department of Anatomy and Anthropology, Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

    The Dr. Miriam and Sheldon G. Adelson Chair and Center for the Biology of Addictive Diseases, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel

    Nikolaos Pitsikas     Department of Pharmacology, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa, Greece

    Luisa Ponzoni     Fondazione Umberto Veronesi, Milan, Italy

    Rui Daniel Prediger

    Department of Pharmacology, Center of Biological Sciences, Universidade Federal de Santa Catarina (UFSC), Campus Trindade, Florianópolis, Brazil

    Graduate Program of Neuroscience, Center of Biological Science, Universidade Federal de Santa Catarina (UFSC), Campus Trindade, Florianópolis, Brazil

    Jos Prickaerts     Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, Maastricht, MD, The Netherlands

    Gustavo Provensi     Department of Neuroscience, Psychology, Drug Research and Child Health, Section of Pharmacology and Toxicology, University of Florence, Florence, Italy

    Doaa Qubty     Department of Anatomy and Anthropology, Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Jacob Raber

    Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United States

    Departments of Neurology and Radiation Medicine, and Division of Neuroscience ONPRC, Oregon Health & Science University, Portland, OR, United States

    Benno Roozendaal

    Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The Netherlands

    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands

    Vardit Rubovitch     Department of Anatomy and Anthropology, Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Mariaelvina Sala     CNR, Institute of Neuroscience, Milan, Italy

    Carla Scali     Kedrion S.p.A., Loc. Il Ciocco, Lucca, Italy

    Shaul Schreiber

    Department of Psychiatry, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel

    Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

    Pascale Schumann-Bard     Normandie Univ., UNICAEN, INSERM, COMETE, Caen, France

    Peter Serrano     Department of Psychology, Hunter College of CUNY, New York, NY, United States

    R.H. Silva     Behavioral Neuroscience Laboratory, Department of Pharmacology, Universidade Federal de São Paulo, São Paulo, Brazil

    Reinaldo Naoto Takahashi     Department of Pharmacology, Center of Biological Sciences, Universidade Federal de Santa Catarina (UFSC), Campus Trindade, Florianópolis, Brazil

    Lisa R. Taxier     Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, WI, United States

    Alvin V. TerryJr

    Department of Pharmacology and Toxicology, Medical College of Georgia, Augusta University, Augusta, GA, United States

    Small Animal Behavior Core, Augusta University, Augusta, GA, United States

    Nick van Goethem     Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, Maastricht, MD, The Netherlands

    Britt T.J. van Hagen     Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, Maastricht, MD, The Netherlands

    Seralynne D. Vann     School of Psychology, Cardiff University, Cardiff, United Kingdom

    Chiara Verpelli     CNR, Institute of Neuroscience, Milan, Italy

    E.C. Warburton     School of Physiology, Pharmacology & Neuroscience, University of Bristol, Bristol, United Kingdom

    Georgia Watt     School of Medicine, Western Sydney University, Campbelltown, NSW, Australia

    Aldis Patrick Weible     Institute of Neuroscience, University of Oregon, Eugene, OR, United States

    Boyer D. Winters

    Department of Psychology, University of Guelph, Guelph, ON, Canada

    Collaborative Neuroscience Program, University of Guelph, Guelph, ON, Canada

    Davide Zoccolan     Visual Neuroscience Lab, International School for Advanced Studies (SISSA), Trieste, Italy

    Preface

    Human and animal environments are constituted with a wide variety of physical objects, which are effortlessly recognized from different viewpoints, in unusual orientations and background noise, at varying scales, under partial occlusion and different illumination conditions. This recognition of objects in the surrounding environment plays an essential role for survival in humans and animals. It has been the most fascinating, but also the most challenging, subject of interest in psychology, neuroscience, engineering and computer sciences. Numerous advances have been made in the understanding of how objects are perceived, encoded, recognized and remembered. These advances have been mostly achieved in humans, primates and birds because of their highly developed visual systems.

    Object recognition in rats and mice has been limited for a number of years to visual pattern discrimination and object novelty-induced neophobia. It gained interest in the last 3  decades with the introduction of the object novelty recognition test which relies on the natural tendency of animals to spend more time exploring a novel object when presented alongside a familiar one (Ennaceur and Delacour, 1987, 1988). It is currently widely popular due to the fact that it is simple to administer, relies entirely on animals' spontaneous exploratory activity without the need for explicit reinforcers and, importantly, can be administered in the same way to rats, mice, nonhuman primates and humans. Because of these attributes, object novelty recognition procedures appear to have supplanted the delayed non-match-to-sample task, which has been the major tool in the study of memory in humans and primates.

    Early interest in object recognition memory in rats and mice was dictated by the need for nonspatial memory tasks that could be used to facilitate the study of medial temporal lobe amnesia reported in humans (Aggleton, 1985; Myhrer, 1988; Mumby et al., 1990; Rothblat and Hayes, 1987). Object novelty recognition was also prompted by the need to eliminate or minimize the use aversive or appetitive reinforcement, the effects of which can be confounded with the effects of an experimental manipulation on learning and memory performance. Hence, the object novelty recognition task has been exploited mainly in memory research. It has been used to determine the brain structures and neural circuits that underlie memory of objects, but is also used in behavioural phenotyping of mouse mutants and in screening for novel disease models and novel therapeutic interventions. It has also been extended to include memory of the location of an object and memory of an episode, and there are now many variants of this test that have been proposed for the investigation of various aspects of memory.

    In the present handbook we aimed to provide an overview of the empirical and theoretical advances achieved with the introduction of the spontaneous object recognition task. The handbook starts with a set of chapters on methods, techniques and test procedures that have been used to assess object novelty recognition memory and other variants of this test. Chapters covering methodological issues and advances in the study of vision and perception of object features and attributes are also included. These are followed with a description of research studies on object recognition in some species other than rodents. The next chapters describe and discuss the role of major brain structures and neurochemical systems in object recognition memory. A set of chapters are then dedicated to aging and animal models of some neuropsychiatric disorders and another set of chapters provides an overview of studies on sex and hormones.

    We hope that the various topics covered in this handbook would further stimulate research to advance our understanding of object recognition in rodents and facilitate the investigation of cognitive processes and neural substrates that supports object novelty recognition.

    We would like to thank all the authors for their valuable contributions to this handbook. We would like to thank also the Elsevier team that supported us throughout the editorial process. Our thanks to Gabriela D. Capille, Anusha Sambamoorthy and Sruthi Satheesh.

    Abdel Ennaceur     Department of Pharmacy, University of Sunderland Wharncliffe Street, Sunderland, United Kingdom

    Maria A. de Souza Silva     Center for Behavioral Neuroscience, University of Düsseldorf, Universitätsstr, Düsseldorf, Germany

    References

    Aggleton J.P. One-trial object recognition by rats. Q. J. Exp. Psychol. B. 1985;37:279–294.

    Ennaceur A, Delacour J. Effect of combined or separate administration of piracetam and choline on learning and memory in the rat. Psychopharmacology (Berl). 1987;92:58–67.

    Ennaceur A, Delacour J. A new one-trial test for neurobiological studies of memory in rats .1. behavioural data. Behav. Brain Res. 1988;31:47–59.

    Mumby D.G, Pinel J.P.J, Wood E.R. Nonrecurring-items delayed nonmatching-to-sample in rats: a new paradigm for testing nonspatial working memory. Psychobiol. 1990;18:321–326.

    Myhrer T. Exploratory behavior and reaction to novelty in rats with hippocampal perforant path systems disrupted. Behav. Neurosci. 1988;102:356–362.

    Rothblat L.A, Hayes L.L. Short-term object recognition memory in the rat: nonmatching with trial-unique junk stimuli. Behav. Neurosci. 1987;101:587–590.

    Chapter 1

    Object Novelty Recognition Memory

    Abdel Ennaceur     Department of Pharmacy, University of Sunderland, Sunderland, United Kingdom

    Abstract

    Object novelty recognition is derived from the spontaneous preference demonstrated towards an object which has not been encountered in the past. This preference of a novel object is the result of the retrieval of stored representations from previous experience of other objects. The stored representation of an object may be constituted from the whole or limited encoded features; it may also comprise the context or some elements of the context in which the object was presented. In rodents, object novelty recognition has been mostly concerned with memory types and processes, and it is only recently that a limited number of research studies started looking at object perception and encoding processes. In this chapter, we will describe the evidence from animal and human literature regarding the object features, the complexity objects, and the similarity between the paired objects and the representation of the familiar object. We will also describe various factors that contribute to encoding and discrimination or recognition of objects. Among these factors are the amount of pretest habituation sessions, changes in locomotor activity and exploration, and changes that may occur from the use of single versus a pair of identical or different objects in the acquisition phase. As discussed in this chapter, the object novelty recognition test has its limitations, particularly regarding the study of object features and working memory which require strict control over the test parameters. This could be resolved with the development of automated visual object recognition tests, which takes into consideration rodents' visual abilities and the consequences of these in the design of a discrimination and a delayed nonmatching-to-sample test apparatus.

    Keywords

    Delayed nonmatching-to-sample; DNMS; Complex object; Object features; Object recognition; Object representation; Object similarities

    1. Introduction

    Thirty years have passed since the first publication that described the object novelty recognition memory test (ONRMT) designed for rats (Ennaceur and Delacour 1987), which was later adopted for mice (Messier 1997; Dodart et al., 1997), and then for other species (Thinus-Blanc et al., 1992; Diamond 1990; Bachevalier et al., 1993; Lorrio et al., 2007; Lucon-Xiccato and Dadda, 2014; Moustgaard et al., 2002; Okujava et al., 2005; Stöwe et al., 2006; Visser et al., 2002; Wood-Gush and Vestergaard 1991). This handbook covers various topics that illustrate the usages and advances made with a memory test, which is based on animals' spontaneous exploratory activity and which exploits their natural preference for novelty. In this chapter, I cover a few minor issues that need addressing and discuss other issues that might be relevant to the analysis and interpretation of results obtained in ONRMT and other variant of this test.

    2. Object Novelty Recognition Memory Test Uses

    The ONRMT was developed mainly as an alternative to the spatial mazes and avoidance conditioning tests which were dominant at that time. Since then, it has been used in a wide range of research studies that used lesions (Dere et al., 2007; Ennaceur and Meliani 1992b; Ennaceur 1998; Ennaceur et al., 1996; 1997a; Ennaceur and Aggleton 1997; Lyon et al., 2012), drugs (Brown et al., 2012; Dere et al., 2007; Ennaceur and Meliani 1992a; Lyon et al., 2012; Prickaerts et al., 2004) and genetic (Dere et al., 2007; Foley et al., 2015; Lyon et al., 2012; Yang et al., 2015a,b; Webster et al., 2014) manipulations or neurochemical (Guzmán-Ramos et al., 2012; Scali et al., 1994; Vannucchi et al., 1997; Moreno-Castilla et al., 2017), histochemical and neuroimaging (Aggleton et al., 2012; Barry et al., 2018; Mansuy et al., 1998; Kelly et al., 2003; Kinnavane et al., 2015) and electrophysiological (Weible et al., 2012; Larkin et al., 2014) techniques. It has been exploited in cross species (Burke et al., 2011; Blaser and Heyser 2015), ontogenetic (Anderson et al., 2004; Cyrenne and Brown 2011; Ramsaran et al., 2016; Westbrook et al., 2014), sexual dimorphism (Bowman et al., 2003; Cyrenne and Brown 2011; Bettis and Jacobs 2012) and ageing (Burke et al., 2011; Traschütz et al., 2017; Vannucchi et al., 1997) studies. It has also been exploited in animal models of various human pathological conditions, such as Alzheimer's disease (Bengoetxea et al., 2015; Grayson et al., 2015; Foley et al., 2015), Parkinson's disease (Magen et al., 2012; Hsieh et al., 2012), traumatic brain injury and cerebrovascular disorders (Hase et al., 2018; Sasaki et al., 2016; Yoshizaki et al., 2008), schizophrenia (Grayson et al., 2015; Lyon et al., 2012; Rajagopal et al., 2014), attention deficit hyperactivity disorder (Heyser et al., 2004; Leffa et al., 2016; LeBlanc-Duchin and Taukulis, 2007), autism (Pilorge et al., 2016; Sungur et al., 2017) and others.

    The ONRMT has been mainly used to assess short- and long-term memories and the process of consolidation/reconsolidation (Bruel-Jungerman et al., 2005; Jessberger et al., 2009; Mansuy et al., 1998; Kelly et al., 2003; de Lima et al., 2005; Rossato et al., 2007; Winters et al., 2011), but has been extended to include spatial memory (Ennaceur et al., 1997a) and lately adapted for episodic memory (Eacott and Norman 2004; Dere et al., 2004), pattern separation and cross-modal recognition (Jeffery 2007; Hindley et al., 2014; Reid et al., 2012; van Hagen et al., 2015).

    3. Diversity and Exploitation of Test Parameters

    The wider exploitations of the ONRMT is mostly due to the fact that the test relies on the spontaneous response of animals to novelty and provides a measure of memory performance without the confounding factors inherent to the use of appetitive or aversive incentive. In addition, the test can be performed in various types of open field, and it can be run in one single session which would take only few minutes, though it is preferable to run two or three sessions, one session a day, to confirm the consistency of memory performance across sessions. Furthermore, the test does not require training animals; hence, it is less labour intensive than the traditional learning and memory tests, and it is far less labour intensive with the current advanced behavioural tracking systems than with manual recording. All these test features did make the ONRMT very appealing to any one from various fields of biomedical sciences. However, with the apparent simplicity of the test and ease of use, there are some concerns regarding the level of expertise in animal behaviour and methodology. While the test eliminated the appetitive and aversive confounds, it relies heavily on locomotor activity; this cannot be ignored and should not be confused with exploratory activity. There is very limited consideration devoted to the pretest habituation procedure (see, Jablonski et al., 2013); this varies widely from one or two sessions (Ameen-Ali et al., 2012; Bianchi et al., 2009; Fernandez et al., 2017; Gaskin et al., 2010; Liu and Bilkey 2001; Schrijver et al., 2002) to three (Jurado-Berbel et al., 2010; Sarkisyan and Hedlund 2009; Sutcliffe et al., 2007; Tanimizu et al., 2017; Traschütz et al., 2017; Westbrook et al., 2014) or even four to seven sessions (Ainge et al., 2006; Bado et al., 2011; Rossato et al., 2013) and lasts between 5 (Sarkisyan and Hedlund 2009), 10 (Ameen-Ali et al., 2012; Gaskin et al., 2010; Westbrook et al., 2014; Traschütz et al., 2017), 20 (Bado et al., 2011; Rossato et al., 2013; Tanimizu et al., 2017) and 30  min (Fernandez et al., 2017). The habituation between the acquisition phase and the choice phase is almost completely ignored. In addition, some studies used one object (Escorihuela et al., 1995; Howlett et al., 2004; Hryniewicz et al., 2007) or either two or more different objects (Benetti et al., 2009; Bozon et al., 2003; Callaghan and Kelly 2012; Rossato et al., 2007; Maroun and Akirav 2008; Myskiw et al., 2008; Wilson et al., 2013; Yamada et al., 2014) in the sample phase as if this method is equivalent to that which involves two identical objects. Furthermore, the test is mostly run in a single test session (Bozon et al., 2003; Herring et al., 2008; Muñoz et al., 2010) and relies on a single discrimination index (Morley et al., 2001; Herring et al., 2008). There is also only a limited number of reports where the total amount of exploration of the objects is controlled (Ainge et al., 2006; Ennaceur and Delacour 1988; Ennaceur and Aggleton 1997; Frick and Gresack 2003; Warburton et al., 2000; Ding et al., 2016) in order to determine the contribution of encoding on memory performance (Ennaceur and Delacour 1988; Ennaceur and Aggleton 1997).

    4. Plurality and Ambiguity of the Object Novelty Recognition Memory Test Identifiers

    ONRMT is currently known by various identifiers. It was at first referred to as object recognition memory test or spontaneous object recognition memory test, but since then it took various names, among which novel object recognition which is widely used. The identification of the test as such seems to have started in 1999 (Besheer et al., 1999; Besheer and Bevins 2000; Tang et al., 1999; Rampon et al., 2000), popularized by molecular neurobiologists during the behavioural phenotyping venture. There is some ambiguity concerning the meaning of novel object recognition test; it could refer to the novelty of the test or to the novelty of the object. The name of the test does not need to be different from identical or comparable tests used in humans and primates, except that in the present case recognition memory is derived from motor exploratory activity of animals. Visual paired comparisons test (Fantz 1964, 1975) is also inappropriate as ONRMT is not limited to vision but includes other sensory modalities for object encoding and recognition. Hence, in order to capture the intended use of Ennaceur and Delacour test, we thought that object novelty recognition would be more appropriate; this would integrate all types of research studies where object novelty is central to all forms of recognition processes.

    5. Object Recognition and Working Memory

    ONRMT was first presented as a working memory test (Ennaceur and Delacour 1987, 1988), but this has yet to be used for that purpose. Working memory is a cognitive system characterized by a limited capacity storage and an executive process which actively hold, update and manipulate incoming information (sensory inputs and retrieved internal representations) for a limited amount of time in response to immediate information processing demands (Baddeley 2010; Baddeley 2012; Cowan 2008; Engle et al., 1999). In rodent research studies, working memory has been attributed mostly to spatial memory tests (Guitar, Roberts 2015; Olton et al., 1977; Olton et al., 1980; Paul et al., 2009), though there are also a number of reports which attributed working memory to the non-spatial one (Aggleton et al., 1986; Mumby et al., 1990). Unlike in humans, working has been defined as short term store (buffer) used to hold representations of selected stimuli (arms, cues or objects) or responses (correct and incorrect choices) until the completion of the behavioural test session. Therefore, evidence of working memory can be demonstrated only in behavioural tests, which are performed in a number of dependent test trials. This is not the case for ONRMT, which is run in a single trial constituted with a sample phase (encoding) and a choice phase (retrieval). Adding another trial or a series of trials (Aggleton 1985; Albasser et al., 2010; Ameen-Ali et al., 2012; Mumby et al., 1990) will not change the function of the test; each trial remains completely independent from another trial in a test session. When performing the ONRMT rodents are not required to hold the memory of the previous sample or the choice object to perform a discrimination in subsequent trials–a trial consists of a sample phase and a choice phase.

    Working memory is likely to be involved when animals have to learn about the features of the objects and have to switch attention from one object to another object during the sample phase and during the test phase (e.g., comparing the actual features of an object to its stored representation or to the representation of another object). It is hard to measure this with the current test procedures, and it is much harder to demonstrate the involvement of working memory bridging between the two phases in just one trial session. However, this can be done in operant conditioning visual object discrimination and recognition paradigms where one can manipulate the components of an object or a scene displayed on a screen monitor (see Section 8.3). As it stands, ONRMT can only be used to examine and assess short- and long-term memories or the memory of an episode.

    6. Object Novelty Recognition Memory Test and Variants

    Since the first version of the ONRMT, a number of test variants have been proposed for assessing different forms of memory and memory processes. One of the first test derived from the ONRMT is the spatial novelty recognition memory test (SNRMT), known as the object location test (Ennaceur et al., 1997a). This provided the chance to assess spatial memory in almost identical conditions to those present in ONRMT, the nonspatial one. The only difference is that in the test phase, one familiar object is replaced by a novel in the ONRMT and one familiar object is displaced to a novel location in the SNRMT. This is a big advantage for cross-comparisons of results between spatial and nonspatial memory tests. The SNRMT was followed with the development of the temporal order memory test (Mitchell and Laiacona 1998), then the object in place and object in context (Dix and Aggleton 1999; Langston and Wood 2010), cross-modal recognition (Reid et al., 2012) and pattern separation (van Hagen et al., 2015) tests. Some of these variants of the object recognition led to the episodic memory tests (Eacott and Norman 2004; Dere et al., 2004; Dere et al., 2005a,b; Kart-Teke et al., 2006). Most of these tests are described in various chapters of this handbook. Here we will consider mainly the two standards tests: the ONRMT and SNRMT.

    7. Open Field and Mazes

    In the ONMRT, animals are exposed to one or two identical objects in an open field, then after a retention interval, they are reexposed to an identical copy of the sample object alongside a novel object. The open field consists of either a square, rectangular or circular field with surrounding walls that are high enough to prevent animals reaching the top edges. In some studies, inclined side walls have been used to avoid having shadows from overhead illumination (Chen et al., 2000; Zanardi et al., 2007), hence reducing animals' preference for these areas. Unfortunately, with even slightly inclined walls animals spend a lot of time trying to climb the walls (see, Ennaceur et al., 2017), particularly if the pretest habituation was limited to one or two short sessions. ONRMT can also be run in open field without walls. In this case, a large platform (at least 80  ×  80  cm) is used. It must be sufficiently elevated from the ground (>70  cm) to avoid animals jumping off the platform. However, animals may get distracted by the edges and would require a number of pretest habituation exposures to the platform (see, Ennaceur et al., 2006, 2009; 2010).

    Mazes have also been used instead of open fields. In this case, the object must be small enough for animals to go around the objects and explore all their parts. This may not be possible with large objects obstructing access to the alleyway. The affordance of small objects is different from that of large objects; for instance, large objects afford shelter and small objects afford grasping (Cos-Aguilera et al., 2004; see Heyser and Chemero 2012). When using mazes, a significant difference in the size of the objects do lead to significant difference in recognition performance (Cassaday and Rawlins 1995; Higgs et al., 2001; Rawlins et al., 1993) and to seemingly conflicting results between studies. The alleyway may appear as a box with either small or large inserts. With small objects, animals would be able to explore not only most parts of the objects but also the inside of the alley, whereas with large objects, animals would be able to explore the front and may be the top side.

    8. Object Features

    Memory performance in ONRMT and its variants depends on the object features, which would determine how an object could be discriminated or recognized. Shape, size, colour, brightness, texture and odours are the features of an object; they contribute either separately or in combination to discrimination and recognition performance.

    A wide and diverse range of objects have been used in ONMRT and other variants of this test. Some objects consisted of a variety of household items such as bottles, cans, boxes, jars, candlesticks and toys made of plastic or aluminium. Some objects were constructed from Lego bricks, while others were constructed from solid materials and designed in some particular shapes (cubes, pyramids and cylinders). The shape, size, colour and materials of these objects are also diverse and mostly composite. In addition, some objects are the size of a marble ball or a bolt, and other objects are of the same height of mouse or a rat. The selection of these objects is mainly the experimenter's personal choice, and there is no much attention paid to the features of the paired objects. Two objects that appear to us to differ in shapes and colours may not be visually distinguishable at all on the basis of these features and may be encoded by animals according to only one of these two features (see Section 8.1) or other sensory features afforded by the object (Albasser et al., 2010; Braida et al., 2013; Moreno et al., 2010; Vasconcelos et al., 2011; Winters and Reid 2010).

    When discussing object features, the focus has been generally on the visual aspects of the objects with very limited considerations to textures and odours. In regard to odours, most authors were concerned by olfactory trails rather than odours that are inherent, particular to an object. We expect that in the near future, with further development in the study of cross-modal recognition (Winters and Reid, 2010; Hindley et al., 2014), we would learn more about object feature recognition. It is worthwhile to consider the present available references on visual recognition as some elements of this could be relevant to object novelty recognition. Furthermore, one has to recognize the limitations of object novelty recognition tests in rodents, which are run manually, and therefore provide reduced control of the test parameters. Various aspects of object recognition need to be examined in automated visual recognition paradigms; it has been started recently with the study of object features and invariant object representations (Alemi-Neissi et al., 2013; Bossens and Op de Beeck 2016; Rosselli et al., 2015; Vermaercke and Op de Beeck 2012; Zoccolan et al., 2009; Zoccolan 2015), and it is highly likely that soon we will be able to examine encoding processes in working memory as well. ONRMT may still continue to retain the advantages of natural preference and spontaneity.

    8.1. Visual Features

    Vision studies in rodents indicated that objects could be encoded on the basis of a very limited number of features despite their apparent complexity. It has been reported that in a discrimination test, rats may rely on local luminance differences in the lower hemifield (Minini and Jeffery 2006; Simpson and Gaffan 1999; Vermaercke and Op de Beeck 2012; Zoccolan et al., 2009; Zoccolan 2015). Similar strategy was observed with rhesus monkeys; they use particular spatial regions in complex scenes (Nielsen et al., 2006). Furthermore, in Lashley jumping stand, rats demonstrated difficulties in discrimination between a triangle and a square with identical base-lines though they were able to discriminate between an inverted triangle and a square (Lashley 1938b; see, Dodwell 1957; Fields 1932). In the former, the triangle and the square had similar lower parts which were not the case in the latter with the inverted triangle. Comparable results were found in pigeons (Towe 1954) and chicken (Munn 1931). There is only a limited number of studies that looked at which physical features rats and mice use when making a discrimination between objects (Alemi-Neissi et al., 2013; Bossens and Op de Beeck 2016; De Keyser et al., 2015; Rosselli et al., 2015; Vermaercke and Op de Beeck 2012; Zoccolan et al., 2009; Zoccolan 2015). When exposed to an object a rat or a mouse may consider only a single feature of an object or a small part of the object that could be used to discriminate this from another object. This is not an issue when animals continue to discriminate between a pair of objects at short retention intervals. However, with the encoding of one particular feature of an object, memory of that object is likely to be weak and susceptible to interferences. After a certain period of time has elapsed, it is not possible to call upon the other features of the object as they were ignored.

    8.2. Visual Stimuli Affordances

    When using objects, animals can view and sense the objects from a distance but have also the chance to approach and sample the objects from proximity. However, when using visual stimuli on screen monitor, there is an assumption that rats and mice had the opportunity to watch the full content of the display, and on this basis, they were able to choose the novel from the familiar or to choose the rewarded from the nonrewarded stimulus. With the limitations to their binocular vision and nothing that prevents them being too close to the visual display, it is surprising that they can afford the whole visual characteristics of the stimuli that they have to encode and recognize, particularly on a vertical flat screen. In mouse vision research, the limitations of flat screen monitor is well recognized. Busse describes some of the attempts that have been made to overcome these limitations (see Chapter 4, section 3 in this volume).

    Rats appear to have limited abilities to focus light from different distances or angles (Artal et al., 1998). Their visual acuity is 1.2 c/d (cycles/degree) in pigmented rats and 0.34–0.43 c/d in albino rats (Birch and Jacobs 1979; Jacobs et al., 1982, 2001). Optimal viewing distance seems to vary between reports. In one report, the distance used ranged from 20 to 30  cm (Wiesenfeld and Branchek, 1976), and in another report, it ranged from 30 to 160  cm (Dean 1981). According to Dean (1981), this variability could be explained by the fact that varying the distance of the stimulus also varied the angle that it subtended at the rat's eye. Hence, it is surprising to read that rodents can discriminate and recognize between briefly presented visual stimuli without any control of their viewing distance. Left free and motivated by food reward, rats and mice are mostly at a touching distance from the display monitor (Leach et al., 2016; Silverman et al., 2015; Turner et al., 2017; Reinagel 2013; but see Markham et al., 1996). As mentioned earlier, rats or mice could have resolved discrimination between visual stimuli based on very limited details of the displayed cues. It is also possible that, due to the considerable length of shaping and training required, rats and mice may have learnt to resolve the discrimination challenge by other means undetectable to an observer. If rats did not use some form of strategy, why are they able to achieve a high level of performance in various, and even complex, operant visual discrimination tasks (Andrews et al., 1992; Carli et al., 1983; Evenden et al., 1989; Cole and Robbins 1987; Reinagel 2013; Alemi-Neissi et al., 2013; Rosselli et al., 2015) but remain unable to perform an operant visual recognition memory task, even at short retention delays?

    Rats and mice have eyes located laterally; they appear to have limited binocular vision (Hughes 1977a,b; 1979; Sefton et al., 2004). The use of a single flat vertical screen display ignores the consequences of this anatomical constraint on rodents' vision and visual perception. The lateral location of the eyes provides a hemipanoramic vision that includes a narrow central binocular zone, flanked by larger monocular zones (Priebe and McGee 2014). The overlap of the fields of the two eyes for binocular vision is estimated to be 40–60  degrees (Sefton et al., 2004). According to Priebe and McGee (2014), the visual world seen by both eyes in front of the mouse is small, and that the mouse visual system is devoted mostly to monocular than binocular vision. This monocular vision in rats and mice accounts for the movements of the head back and forth and from side to side when at a distance from an object or a visual stimulus or at the intersection of the arms of a maze. This behaviour reported by Tolman (1926; 1927) was coined ‘vicarious trial and error’ (VTE) by Muenzinger (1938) and adopted by Tolman (1938). VTE refers to the behaviour of rats exhibiting head movements, swinging their head from side to side, at choice points between visual stimuli in a discrimination learning paradigm. It has been thought to reflect approach–avoidance responses, hesitations or decision-making process (Amemiya and Redish 2016; Bimonte and Denenberg 2000; Bett et al., 2012; Crannell 1942; Schmidt et al., 2013), though it can represent simply a visual scanning behavior (Campbell 1956; Dennis and Russell 1939; see also Sahibzada et al., 1986). Indeed, some authors suggested that head movements could reflect a behavioural strategy for sensory fusion of two retinal images into one percept or to achieve stereoscopic depth perception (Meier and Dieringer 1993; Dieringer and Meier, 1993; Kral 2003). It is also observed in laterally eyed species (Kral 1998; Dawkins 2002). Based on the above considerations, we proposed an operant chamber that would resolve the problems encountered by rats in performing delayed nonmatching-to-sample (DNMS) tasks with visual stimuli in automated behavioural test apparatuses.

    8.3. Automated Visual Discrimination and Recognition Memory

    Twenty years ago, we proposed an operant chamber (Fig. 1.1A) which was designed in consideration of the lateral position of the rat eyes and the consequences of this on their visual perception (Ennaceur and Aggleton 1998b). The chamber had three separate small screen displays (about 12 cm wide x 9 cm high). One screen was presented centred on the back wall, whereas the other two were attached either side on opposite walls at obtuse angles. The top of each monitor was moved slightly forward to produce a downward incline. The sample and the choice stimuli did not share the same display medium. Two of the three screens could be randomly selected to display a single stimulus each. Therefore, the stimuli were clearly distinguishable from one another. In addition, animals were forced to stay at least 16  cm away facing the display monitors as they had to press on retractable lever before climbing a stand to reach the selected screen. Hence, the position and orientation of the monitors as well as the forced distance from the screen provided the opportunity for rats to view the stimuli displayed on two separate screen displays before making a choice for a particular stimulus. This apparatus was used to assess delayed nonmatching-to-position (DNMP), and the performance of rats was above 70% from the fifth session (Fig. 1.1C; Ennaceur and Aggleton, 1998a,b). The same level of performance was achieved in a discrimination test between two visual stimuli, which is far faster than in studies on vision where rats are trained for more than 3  weeks to achieve ≥70% correct responses (Alemi-Neissi et al., 2013; Reinagel 2013; Leach et al., 2016; Silverman et al., 2015; Turner et al., 2017). In both DNMP and visual discrimination, there were no pretraining stages. In our early prototype (Ennaceur et al., 1997b), we tested rats in a DNMS. We used three matrices 10  ×  10  cm instead of screen monitors. Each matrix was filled with miniature LED bulbs which were controlled through a computer program to produce various shapes. With this setting, pigmented PVG rat strain was able to acquire DNMS at 0  sec delay. However, with the limitations of the LED matrix displays and the type of visual stimuli produced by these, memory performance was inconsistent between delays and between test sessions. The percent correct response was either at chance level or significantly above chance (≥60% correct) for each individual rat at any retention delay interval. We mean here that in a session, we observed rats achieving ≥70% correct response at any delay in one session and ≈50% correct response for the same delay in another session–the maximum retention delay was only 12 sec.

    Figure 1.1  Illustration (A) of an operant chamber for assessing visual discrimination and recognition memory in rodents. Note here the positions of the retractable levers. They are 16 cm away from the screen displays. There are 3 of them; they can be used for complex testing procedures. The graph on the top right (B) describes the upper and lowest 95% CI obtained over 5 test sessions by rats tested in a DNMS at 0 to 12 sec. mixed retention delays. The group average is indicated with a dotted line and close circles. The graph on the bottom left (C) describes results obtained in a DNMP test. After pressing the central retractable lever, rats had to climb on the platform and approach one the two visual displays (the middle one was off and unused during the test). Then, they had to press either on the left or the right food dispenser underneath the visual display to indicate their choice stimulus. In the contiguous condition (CTG), rats received a food pellet for correct response from the food dispenser that they activated, which was underneath the correct visual stimulus. In the noncontiguous condition (nCTG), rats received a food pellet from the food dispenser underneath the middle display which was off during the test [ Ennaceur and Aggleton 1998a ]. Most operant conditioning tests have been using the non-contiguous conditions. The graph on the bottom right (D) describes results with mixed retention intervals obtained in a DNMP with a test procedure in which the entry to the operant chamber was on the side of one display monitor (Cue condition group) instead of being in front facing the 3 screen monitors (NoCue condition group). The entrance door was made of Perspex Plexiglas [ Ennaceur and Aggleton 1998a ]. Here again, most operant conditioning tests have the access door located on the side adjacent to one of the stimuli presented to rats or mice. * p≤0.05; + p≤0.06.

    9. Simple Versus Complex Objects Versus Similarity

    A number of studies suggested that animals spend more time with complex objects than with simple objects and express a preference for the more complex of the two stimuli (Baker and Franken 1967; Dember and Earl 1957; Dember et al., 1957; Denny 1975; Dutch and Brown 1971; Sales 1968; Leyland et al., 1976; Liu and Bilkey 2001). They suggested also that the preference for complex object follows an inverted-U function, with optimum preference for moderate complex stimuli (Dember and Earl 1957; Sales 1968; French 1954; but see Snodgrass and Vanderwart, 1980). Similar preference for complex objects was observed in human infants (Cheatham et al., 2006; Oakes and Tellinghuisen, 1994; Courage et al., 2004; Ruff 1986; Ruff et al., 1992), with older infants showing preference for more complex objects than younger infants (Bova et al., 2007; Hunter et al., 1983; Juttner et al., 2006; Brennan et al., 1966; Fagan 1990; Fantz et al., 1975; Karmel 1969). Eye movement studies indicate that the object with greater visual complexity attracted fixations earlier and for longer durations (Underwood et al., 2007).

    Complex objects may require greater amounts of exploration or encoding than simple objects (Alvarez and Cavanagh 2004; Awh et al., 2007; Eng et al., 2005; Voss et al., 2017), and therefore for the same short amount of time allocated to explore an object, memory performance would be less accurate and decline faster for complex objects than for simple ones. Indeed, a number of studies reported that visual short-term memory capacity is limited by the complexity or the number of features of the items stored (Brady et al., 2016; Alvarez and Cavanagh, 2004; Wheeler and Treisman, 2002; Olsson and Poom 2005; Kibbe and Leslie 2008; Gao et al., 2008), that the duration of encoding increases with increasing object complexity (Alvarez and Cavanagh, 2004; Awh et al., 2007; Eng et al., 2005; Ouimet and Jolicœur 2007), and that memory performance declines with increasing object complexity (Alvarez and Cavanagh 2004; Brady et al., 2016; Gámiz and Gallo 2012; Eng et al., 2005; Luria et al., 2010). This storage capacity and memory performance apply to complex but meaningless objects (Alvarez and Cavanagh 2004; Brady et al., 2016; Olsson and Poom 2005) but not to real-world complex objects which can benefit from long-term memory of stored perceptual or semantic knowledge about the different features of objects (Baddeley 2010; Ericsson and Kintsch 1995; Postle 2015). For laboratory animals, which have been confined to a small space over a number of generations, such benefit from long-term storage can be very limited or inexistent – all depends on the housing conditions and previous training experience. Hence, what one may call real-world simple or complex objects are mostly meaningless objects to animals. Animals bred in enriched environment may have the chance to experience the features of some objects in their cages, but they may not be able to recognize most of these features in a larger space. The experience of an object in close contact is likely to be different from the experience of an object held at some distances, particularly due to the visual competence of the species and the view perspectives of an object (Artal et al., 1998; Jacobs et al., 2001; Creel et al., 1970; Keller et al., 2000; Lashley 1938a,b; Lashley 1970; Legg and Lambert 1990; O'Sullivan and Spear 1964; Routtenberg and Glickman 1964; Wiesenfeld and Branchek 1976).

    The majority of animal studies on recognition memory refer to simple objects as those with the lowest number of features and complex objects as those with the largest number of features. In a number of studies, simple objects can be identified by at least two features: a shape and a colour (Cassaday and Rawlins 1995; Liu and Bilkey 2001). They are considered simple objects because they are presented in a discrimination or recognition test alongside another object, which differs in either the shape or the colour, or presented alongside an object with more than two features. In this case, recognition memory would be based on interobject similarity than object complexity (Makovski and Yuhong 2008; Wang and Bingo 2010; Newell 1998). Recognition performance is faster and more efficient with low interobject similarity, and it is poor with high interobject similarity (Edelman, 1995; Kobatake et al., 1998; Newell, 1998; Tokudome and Wang 2012; Tranel et al., 1997; Wang and Bingo 2010; Yuhong et al., 2008; Zeamer et al., 2011). In the latter, extensive training would increase the differentiation between objects, hence improve object recognition (Kobatake et al., 1998).

    Objects are discriminated and recognized on the basis of

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