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Postnatal development of the hippocampal formation: neuroanatomical and plasticity studies in monkeys

Applicant Lavenex Pierre
Number 124536
Funding scheme SNSF Professorships
Research institution Division de Physiologie Département de Médecine Université de Fribourg
Institution of higher education University of Fribourg - FR
Main discipline Neurophysiology and Brain Research
Start/End 01.08.2009 - 30.09.2011
Approved amount 781'148.00
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Keywords (7)

memory; hippocampus; amnesia; development; autism; epilepsy; schizophrenia

Lay Summary (English)

Lead
Lay summary
The hippocampal formation is comprised of a group of brain regions located in the medial temporal lobe. Damage to these structures causes a profound loss of memory for events (such as the memories of your wedding or your 20th birthday) and facts about the world (such as the name of the capital of France or the color of the Swiss flag), without other sensory, motor or cognitive impairments. Over the last 30 years, the work of many laboratories worldwide has clarified the basic functional organization of the adult primate hippocampal formation. These fundamental neuroanatomical studies carried out in the monkey have served as the foundation for our understanding of human memory function, and have been essential to our current understanding of the pathology of neuropsychiatric disorders including amnesia, schizophrenia, Alzheimer's disease and epilepsy.The next frontier facing neuroscientists is understanding the neurobiological bases of the development of memory processes, and how the abnormal development of medial temporal lobe structures contributes to the etiology of neurodevelopmental and genetic disorders such as autism and schizophrenia.Our overall research program is integrative and multidisciplinary, focusing on the postnatal neuroanatomical and functional maturation of the primate hippocampal formation with the principal goals of understanding the neurobiological basis of memory processes and the etiology of human neurodevelopmental disorders. The data generated by our research program will provide a comprehensive picture of the maturity of the primate hippocampal formation at birth, as well as the ages at which a variety of neuroanatomical features achieve adult characteristics. By determining when such developmental milestones occur, we will be able to suggest ages at which specific hippocampal circuits are able to subserve specific memory processes. Our studies will also characterize the structural reorganization of the brain that enables functional recovery following early, but not late, hippocampal damage. Our findings will have broad implications for our understanding of human memory processes across the lifespan. Our research carried out in the monkey will also define processes, substrates and critical periods of maturation that might be particularly sensitive to perturbation and contribute to developmental and genetic disorders of the human nervous system such as autism, schizophrenia and epilepsy.
Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Neuroanatomic organization and fundamental dunctions of the hippocampus and th amygdala
Lavenex P (2011), Neuroanatomic organization and fundamental dunctions of the hippocampus and th amygdala, in Riva D et al (ed.), John Libbey Eurotext, London, 89-118.
Postnatal development of the amygdala: A stereological study in macaque monkeys.
Chareyron Loïc J, Lavenex Pamela Banta, Amaral David G, Lavenex Pierre (2011), Postnatal development of the amygdala: A stereological study in macaque monkeys., in The Journal of comparative neurology, 1-21.
Stereological analysis of the rat and monkey amygdala.
Chareyron Loïc J, Banta Lavenex Pamela, Amaral David G, Lavenex Pierre (2011), Stereological analysis of the rat and monkey amygdala., in The Journal of comparative neurology, 519(16), 3218-39.
As the world turns: short-term human spatial memory in egocentric and allocentric coordinates.
Banta Lavenex Pamela, Lecci Sandro, Prêtre Vincent, Brandner Catherine, Mazza Christian, Pasquier Jérôme, Lavenex Pierre (2011), As the world turns: short-term human spatial memory in egocentric and allocentric coordinates., in Behavioural brain research, 219(1), 132-41.
Postnatal development of the hippocampal formation: a stereological study in macaque monkeys.
Jabès Adeline, Lavenex Pamela Banta, Amaral David G, Lavenex Pierre (2011), Postnatal development of the hippocampal formation: a stereological study in macaque monkeys., in The Journal of comparative neurology, 519(6), 1051-70.
Developmental regulation of gene expression and astrocytic processes may explain selective hippocampal vulnerability.
Lavenex Pierre, Sugden Steven G, Davis Ryan R, Gregg Jeffrey P, Lavenex Pamela Banta (2011), Developmental regulation of gene expression and astrocytic processes may explain selective hippocampal vulnerability., in Hippocampus, 21(2), 142-9.
Spatial relational learning and memory abilities do not differ between men and women in a real-world, open-field environment.
Banta Lavenex Pamela, Lavenex Pierre (2010), Spatial relational learning and memory abilities do not differ between men and women in a real-world, open-field environment., in Behavioural brain research, 207(1), 125-37.
Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus.
Jabès Adeline, Lavenex Pamela Banta, Amaral David G, Lavenex Pierre (2010), Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus., in The European journal of neuroscience, 31(2), 273-85.
Spatial memory and the monkey hippocampus: not all space is created equal.
Banta Lavenex Pamela, Lavenex Pierre (2009), Spatial memory and the monkey hippocampus: not all space is created equal., in Hippocampus, 19(1), 8-19.
Neuroanatomy methods in humans and animals
Lavenex P (2009), Neuroanatomy methods in humans and animals, in Squire L (ed.), Academic Press, San Diego, 269-278.
Postmortem changes in the neuroanatomical characteristics of the primate brain: hippocampal formation.
Lavenex Pierre, Lavenex Pamela Banta, Bennett Jeffrey L, Amaral David G (2008), Postmortem changes in the neuroanatomical characteristics of the primate brain: hippocampal formation., in The Journal of comparative neurology, 512(1), 27-51.
Intrinsic connections of the macaque monkey hippocampal formation: I. Dentate gyrus.
Kondo Hideki, Lavenex Pierre, Amaral David G (2008), Intrinsic connections of the macaque monkey hippocampal formation: I. Dentate gyrus., in The Journal of comparative neurology, 511(4), 497-520.
Effects of neonatal amygdala or hippocampus lesions on resting brain metabolism in the macaque monkey: a microPET imaging study.
Machado Christopher J, Snyder Abraham Z, Cherry Simon R, Lavenex Pierre, Amaral David G (2008), Effects of neonatal amygdala or hippocampus lesions on resting brain metabolism in the macaque monkey: a microPET imaging study., in NeuroImage, 39(2), 832-46.
Postnatal development of the primate hippocampal formation
Lavenex P, Lavenex PB, Amaral DG (2007), Postnatal development of the primate hippocampal formation, in DEVELOPMENTAL NEUROSCIENCE, 29(1-2), 179-192.
The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies).
Amaral David G, Scharfman Helen E, Lavenex Pierre (2007), The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies)., in Progress in brain research, 163, 3-22.
Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys.
Lavenex Pierre, Lavenex Pamela Banta, Amaral David G (2007), Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys., in Nature neuroscience, 10(2), 234-9.
Hippocampal neuroanatomy
Amaral DG, Lavenex P (2007), Hippocampal neuroanatomy, in Andersen et al. (ed.), Oxford University Press, Oxford, 37-114.
The expression of social dominance following neonatal lesions of the amygdala or hippocampus in rhesus monkeys (Macaca mulatta).
Bauman M D, Toscano J E, Mason W A, Lavenex P, Amaral D G (2006), The expression of social dominance following neonatal lesions of the amygdala or hippocampus in rhesus monkeys (Macaca mulatta)., in Behavioral neuroscience, 120(4), 749-60.
Hippocampal lesion prevents spatial relational learning in adult macaque monkeys.
Lavenex Pamela Banta, Amaral David G, Lavenex Pierre (2006), Hippocampal lesion prevents spatial relational learning in adult macaque monkeys., in The Journal of neuroscience : the official journal of the Society for Neuroscience, 26(17), 4546-58.
Spatial relational memory in 9-month-old macaque monkeys.
Lavenex Pierre, Lavenex Pamela Banta (2006), Spatial relational memory in 9-month-old macaque monkeys., in Learning & memory (Cold Spring Harbor, N.Y.), 13(1), 84-96.
Functional anatomy, development and pathology of the hippocampus
Lavenex P, Functional anatomy, development and pathology of the hippocampus, in Bartsch T (ed.), Oxford University Press, Oxford.

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Winter Learning and Memory Conference 04.01.2012 Park City, Utah
SFN meeting 2011 11.11.2011 Washington DC
Proteomics and Connectomics Conference 06.07.2011 Fribourg
Spring Hippocampal Research Conference 21.05.2011 Verona
Swiss Society for Neuroscience Meeting 2011 26.03.2011 Basel
Recherche pour la Vie - Déclaration de Bâle 29.11.2010 Basel
Adult neurogenesis conference 27.05.2010 Germany
Swiss Society for Neuroscience Meeting 2010 12.03.2010 Lausanne
Winter Learning and Memory Conference 07.01.2010 Park City, Utah
SFN meeting 2009 17.10.2009 Chicago
Spring Hippocampal Research Conference 13.06.2009 Verona, Italy
SSN /FENS meeting 2008 12.06.2008 Geneva
Swiss Society for Neuroscience Meeting 2007 09.03.2007 Bern
Swiss Society for Neuroscience Meeting 2006 28.01.2006 Basel


Self-organised

Title Date Place
Swiss Society for Neuroscience Meeting 2009 14.03.2009 Fribourg

Awards

Title Year
Research Prize of the Swiss Society for Neuroscience 2010

Associated projects

Number Title Start Funding scheme
143956 Postnatal development and plasticity of the primate hippocampal formation 01.01.2013 Project funding
106701 Postnatal development of the hippocampal formation: neuroanatomical studies in the monkey 01.08.2005 SNSF Professorships

Abstract

The overarching goal of my research program is to understand the neurobiological basis of episodic memory, the memory for autobiographical events. One particularly pertinent conundrum regarding human memory is the fact that until 4 or 5 years of age children do not have the ability to remember specific episodes of their life. Although this phenomenon, known as infantile amnesia, has been the focus of intensive psychological investigation, its neurobiological basis is not understood. In adults, it is well-known that the hippocampal formation is the center of a brain network critical for episodic memory, and damage to the hippocampus results in amnesia, a total loss of memory. Is it possible, then, that the emergence of episodic memory in children depends on the structural and functional maturation of these brain areas?Understanding the postnatal development of the primate hippocampal formation is equally pertinent for understanding the root of neurodevelopmental and genetic disorders, such as autism, schizophrenia and epilepsy, in which developmental abnormalities in these structures are implicated. Although the structures of the primate hippocampal formation are easily recognizable at birth, they undergo substantial postnatal maturation throughout infant and juvenile life. It is therefore logical that during this critical maturational period, these structures are particularly sensitive to intrinsic and environmental factors capable of modulating the expression of particular genes, thus affecting normal brain development and cognition. Data from my research program elucidating the normal development of the primate hippocampal formation are therefore essential to defining processes, substrates and critical periods of maturation that are sensitive to perturbation and contribute to the etiology of neurodevelopmental disorders.In the current funding period, we have focused on the postnatal neuroanatomical maturation of the primate hippocampal formation with the principal goal of describing the development of the neurobiological substrates thought to subserve the emergence of episodic memory. The project had two complementary experimental aims: (1) To determine, using stereological techniques, the ages at which principal neurons in the different regions of the monkey hippocampal formation achieve adult morphological characteristics; and (2) to determine the ages at which the major neurotransmitter systems are neurochemically mature in distinct and specific circuits of the monkey hippocampal formation. In both aims, we have made significant progress that I will describe in more detail below. The data already generated by my research program has provided critical new information regarding the maturity of the primate hippocampal formation at birth, as well as about the ages at which a variety of neuroanatomical features achieve adult characteristics.This new application builds on the results obtained in the current funding period and is the next critical step in the multi-step (and multi-year) process that will ultimately lead to a greater understanding of the development, plasticity and function of the primate hippocampal formation. The proposed project has two complementary experimental aims: (1) To further characterize the normal neuroanatomical maturation of the monkey hippocampal formation during early postnatal development; and (2) to characterize the structural reorganization of the medial temporal lobe structures that enables functional recovery following early, but not late, hippocampal lesions.
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