Project

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Postnatal development and plasticity of the primate hippocampal formation

English title Postnatal development and plasticity of the primate hippocampal formation
Applicant Lavenex Pierre
Number 143956
Funding scheme Project funding
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 01.01.2013 - 31.12.2015
Approved amount 445'000.00
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Keywords (4)

plasticity; development; hippocampus; memory

Lay Summary (English)

Lead
Lay summary

The hippocampal formation is essential for the processing of declarative memory, which includes the representation of unique personal experiences called episodic memories and the memory for facts about the world called semantic memories. In humans, significant changes in the capacity for declarative memory occur within the first 3-7 years of life, but the neurobiological basis for such changes had remained highly hypothetical. In the last few years, however, our own studies have demonstrated that distinct regions, layers and cells of the hippocampal formation exhibit different profiles of structural development during early postnatal life. Together with functional studies of memory, our findings suggested how the differential maturation of distinct hippocampal circuits might underlie the emergence of specific "hippocampus-dependent" memory processes, culminating in the emergence of episodic memory concomitant with the maturation of all hippocampal circuits.

This application builds on the results obtained in previous years and will contribute to approaching our long-term goal of understanding the development, plasticity and function of the primate hippocampal formation.

In the first project, we will test the hypothesis that distinct layers and subdivisions of the primate entorhinal cortex, which contribute to different hippocampal functional circuits, exhibit differential maturation during early postnatal development. We already obtained preliminary evidence showing that the superficial layers II and III mature earlier that the deep layers V and VI. This suggests that although neocortical inputs can reach and be processed within hippocampal circuits relatively early, hippocampus output might be directed preferentially toward subcortical structures at early ages, and only reach neocortical areas at later stages of postnatal development.

In the second project we will test the hypothesis that, following neonatal hippocampal damage, the medial temporal lobe memory system undergoes structural and functional reorganization to enable the acquisition of long-term spatial memories. We have already found preliminary evidence of such reorganization at both structural (neuroanatomical tracers) and functional (immediate-early gene experiments) levels.

Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Stereological analysis of the rhesus monkey entorhinal cortex
Piguet Olivia, Chareyron Loïc J., Banta Lavenex Pamela, Amaral David G., Lavenex Pierre (2018), Stereological analysis of the rhesus monkey entorhinal cortex, in Journal of Comparative Neurology, 526(13), 2115-2132.
Functional organization of the medial temporal lobe memory system following neonatal hippocampal lesion in rhesus monkeys
Chareyron Loïc J., Banta Lavenex Pamela, Amaral David G., Lavenex Pierre (2017), Functional organization of the medial temporal lobe memory system following neonatal hippocampal lesion in rhesus monkeys, in Brain Structure and Function, 222(9), 3899-3914.
Selective lesion of the hippocampus increases the differentiation of immature neurons in the monkey amygdala
Chareyron Loïc J., Amaral David G., Lavenex Pierre (2016), Selective lesion of the hippocampus increases the differentiation of immature neurons in the monkey amygdala, in Proceedings of the National Academy of Sciences, 113(50), 14420-14425.
An analysis of entorhinal cortex projections to the dentate gyrus, hippocampus, and subiculum of the neonatal macaque monkey.
Amaral David G, Kondo Hideki, Lavenex Pierre (2014), An analysis of entorhinal cortex projections to the dentate gyrus, hippocampus, and subiculum of the neonatal macaque monkey., in The Journal of comparative neurology, 522(7), 1485-505.
What animals can teach clinicians about the hippocampus.
Lavenex Pierre, Banta Lavenex Pamela, Favre Grégoire (2014), What animals can teach clinicians about the hippocampus., in Frontiers of neurology and neuroscience, 34, 36-50.
Building hippocampal circuits to learn and remember: Insights into the development of human memory
Lavenex Pierre, Banta Lavenex Pierre (2013), Building hippocampal circuits to learn and remember: Insights into the development of human memory, in Behavioural Brain Research, 254, 8-21.

Collaboration

Group / person Country
Types of collaboration
Dr. David Amaral / UC Davis United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Swiss Society for Neuroscience Meeting Poster Quantitative analysis of the structural organization of the monkey entorhinal cortex 23.01.2016 Lausanne, Switzerland Lavenex Pierre; Chareyron Loïc;
American Society for Neuroscience Meeting Poster Functional reorganization of the medial temporal lobe memory system following neonatal hippocampal damage in monkeys 20.10.2015 Chicago, United States of America Chareyron Loïc; Lavenex Pierre;
American Society for Neuroscience Meeting Poster Lesion-induced brain plasticity: Massive increase in neuron number in the monkey amygdala following early or late hippocampal lesion. 20.10.2015 Chicago, United States of America Chareyron Loïc; Lavenex Pierre;
Swiss Society for Neuroscience Meeting Poster Functional reorganization of the medial temporal lobe memory system following neonatal hippocampal damage in monkeys 24.01.2015 Fribourg, Switzerland Chareyron Loïc; Lavenex Pierre;
16th European Conference on Developmental Psychology Talk given at a conference Development of allocentric spatial memory abilities in children from 18 months to 5 years of age: a neurobiological perspective 03.09.2014 Lausanne, Switzerland Lavenex Pierre;
FENS meeting Poster Functional reorganization of the medial temporal lobe memory system following neonatal hippocampal damage in monkeys 06.07.2014 Milano, Italy Chareyron Loïc; Lavenex Pierre;
Temple University Research Seminar Series Individual talk How does one (re)build a brain to learn and remember? 18.03.2014 Philadelphia, United States of America Lavenex Pierre;
Annual Meeting of the Eastern Psychological Association Talk given at a conference Postnatal development of memory circuits 13.03.2014 Boston, United States of America Lavenex Pierre;
Swiss Society for Neuroscience Meeting Poster Functional reorganization of the medial temporal lobe memory system following neonatal hippocampal damage in monkeys 25.01.2014 Bern, Switzerland Chareyron Loïc; Lavenex Pierre;
Spring Hippocampal Research Conference Talk given at a conference Memory development 09.06.2013 Taormina, Italy Lavenex Pierre;
Annual Meeting of the Swiss Federation of Clinical Neuroscience Societies Talk given at a conference How does one (re)build a brain to learn and remember? 07.06.2013 Montreux, Switzerland Lavenex Pierre;


Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions La mémoire n'est qu'une illusion Western Switzerland 2018
Media relations: radio, television Mémoire, neurosciences et semaine du cerveau Emission "C'est que du bonheur" Radio Fribourg Western Switzerland 2018
Talks/events/exhibitions Mémoires du temps Western Switzerland 2017
Media relations: print media, online media Cerveau. Il efface les souvenirs de notre petite enfance Science et Vie International 2014
Media relations: print media, online media La mémoire, ses secrets, ses troubles Hors série SCIENCE ET VIE International 2014
Media relations: radio, television L'amnésie infantile Emission CQFD. RTS1 Western Switzerland 2014
Media relations: radio, television Perspective sur le Prix Nobel de Médecine 2014 Emission CQFD, RTS1 Western Switzerland 2014

Associated projects

Number Title Start Funding scheme
124536 Postnatal development of the hippocampal formation: neuroanatomical and plasticity studies in monkeys 01.08.2009 SNSF Professorships
106701 Postnatal development of the hippocampal formation: neuroanatomical studies in the monkey 01.08.2005 SNSF Professorships

Abstract

The hippocampal formation is essential for the processing of declarative memory, which includes the representation of unique personal experiences called episodic memories and the memory for facts about the world called semantic memories. In humans, significant changes in the capacity for declarative memory occur within the first 3-7 years of life, but the neurobiological basis for such changes has so far remained highly hypothetical. In the last few years, we have focused our studies on the postnatal neuroanatomical maturation of the monkey hippocampal formation with the goal of characterizing the development of the neurobiological substrates thought to subserve the emergence of episodic memory. Our studies have provided critical new information regarding the maturity of the primate hippocampal formation at birth and the structural changes occurring during its postnatal development. In particular, we demonstrated that distinct regions, layers and cells of the hippocampal formation exhibit different profiles of structural development during early postnatal life. Together with functional studies of memory, our findings have suggested how the differential maturation of distinct hippocampal circuits might underlie the emergence of specific "hippocampus-dependent" memory processes, culminating in the emergence of episodic memory concomitant with the maturation of all hippocampal circuits.This application builds on the results obtained in the previous funding period and will contribute to approaching our long-term goal of understanding the development, plasticity and function of the primate hippocampal formation. The proposed project aims to test two specific hypotheses:Hypothesis 1: Distinct layers and subdivisions of the primate entorhinal cortex, which contribute to different hippocampal functional circuits, exhibit differential maturation during early postnatal development. The entorhinal cortex is the main gateway for bi-directional communication between the neocortex and the hippocampal formation. Its superficial layers (II and III) represent the main entryways for much of the sensory information processed by the hippocampal formation, whereas its deep layers (V and VI) provide the main exitways through which processed information is sent back to the neocortex. Following our recent neuroanatomical findings revealing differential maturation of distinct hippocampal circuits and the renewed interest in the contribution of the entorhinal cortex in the elaboration of spatial representations of the environment, it is particularly timely and important to obtain fundamental, quantitative information on the structural development of this brain region in primates. We present preliminary evidence showing that the superficial layers II and III mature earlier that the deep layers V and VI. This suggests that neocortical inputs can reach and be processed within hippocampal circuits relatively early, but that hippocampal outputs might be directed mainly toward subcortical structures at early ages, and only reach neocortical areas at later stages of postnatal development.Hypothesis 2: The medial temporal lobe memory system undergoes structural and functional reorganization to enable the acquisition of long-term spatial memories following neonatal hippocampal damage. In the case of human developmental amnesia, patients who sustained hippocampal damage early in life exhibit memory impairments affecting preferentially episodic memory, whereas semantic memory is largely intact. In contrast, lesion of the hippocampus in adults impairs both semantic and episodic memory processes. We have recently shown similar functional plasticity in monkeys that received hippocampal lesions early in life. Hippocampal lesions prevented spatial relational learning in adult-lesioned monkeys, whereas spatial relational learning persisted following neonatal lesions. We will use anterograde and retrograde neuroanatomical tracers to evaluate and characterize the structural reorganization of the monkey medial temporal lobe memory system following early hippocampal lesions. In addition, we will perform quantitative analyses of immediate-early gene (c-fos) expression throughout the brain, following behavioral induction of gene expression via the exploration of a new open-field environment. This project aims to provide experimental evidence of the structural and functional reorganization of the medial temporal lobe memory system that supports spatial learning and memory following early hippocampal damage. We present preliminary evidence of such reorganization in the anticipated results of the detailed research plan.
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