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Parent, André

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  • PublicationRestreint
    Jules Bernard Luys : a singular figure of 19th Century neurology
    (Cambridge University Press, 2002-08-01) Parent, Martin; Parent, André; Leroux-Hugon, Véronique
    Jules Bernard Luys was a highly industrious and dedicated French investigator who made important contributions to the fields of neuroanatomy and neuropsychiatry in the second half of the 19th century. His name is still eponymically attached to the subthalamic nucleus and the centre médian nucleus, two structures that are at the center of our current thinking about the functional organization of the basal ganglia and the pathophysiology of Parkinson’s disease. While developing a highly original view of the anatomical and functional organization of the human brain, Luys contributed significantly to our knowledge of the neuropathological and clinical aspects of mental illnesses. Luys devoted the last part of his career to hysteria and hypnosis, engaging himself in experiments as extravagant as the action of medication at distance. In doing so, he became perhaps the most highly caricatured example of the fascination that hysteria exerted upon various renowned neurologists at the end of the 19th century. This paper briefly summarizes the contribution of this remarkable figure of the history of neurology.
  • PublicationRestreint
    Axonal branching pattern of neurons of the subthalamic nucleus in primates
    (Wistar Institute of Anatomy and Biology, 2000-07-05) Sato, Fumi; Parent, Martin; Parent, André; Lévesque, Martin
    Axonal projections arising from the subthalamic nucleus (STN) in cynomolgus monkeys (Macaca fascicularis) were traced after labeling small pools (5-15 cells) of neurons with biotinylated dextran amine. Seventy-five single axons were reconstructed from serial sagittal sections with a camera lucida. Most of the STN labeled cells displayed five to eight long, sparsely spined dendrites that arborized mostly along the main axis of the nucleus. Based on their axonal targets, five distinct types of STN projection neurons have been identified: 1) neurons projecting to the substantia nigra pars reticulata (SNr), the internal (GPi) and external (GPe) segments of the globus pallidus (21.3%); 2) neurons targeting SNr and GPe (2.7%); 3) neurons projecting to GPi and GPe (48%); 4) neurons targeting GPe only (10.7 %); and 5) neurons with axons that coursed toward the sriatum, but whose terminal arborization could not be visualized in detail (17.3%). Axons of the first two types bifurcated into rostral subthalamopallidal and caudal pallidonigral branches. However, the majority of STN axons had only a single branch that coursed rostrally toward the pallidum and striatum. These results reveal that, in contrast to current beliefs, the primate STN is not a monolithic entity. This nucleus harbors several subtypes of projection neurons, each endowed with a highly patterned set of collaterals. This organization allows STN neurons to exert a multifarious effect not only on the GPe, with which the STN is reciprocally connected, but also on the two major output structures of the basal ganglia, the SNr and the GPi.
  • PublicationRestreint
    Organization of the basal ganglia : the importance of axonal collateralization
    (Elservier, 2004-10-13) Gauthier, Julie; Sato, Fumi; Wu, Martin; Parent, Martin; Parent, André; Lévesque, Martin
    Recent neuroanatomical data obtained with single-axon or single-cell labeling procedures in both rodents and primates have revealed the presence of various types of projection neurons with profusely collateralized axons within each of the major components of the basal ganglia. Such findings call for a reappraisal of current concepts of the anatomical and functional organization of the basal ganglia, which play such a crucial role in the control of motor behavior. The basal ganglia now stand as a widely distributed neuronal network, whose elements are endowed with a highly patterned set of axon collaterals. The elucidation of this finely tuned network is needed to understand the complex spatiotemporal sequence of neural events that ensures the flow of cortical information through the basal ganglia.
  • PublicationRestreint
    A re-evaluation of the current model of the basal ganglia
    (Elsevier, 2001-07-01) Parent, Martin; Parent, André; Lévesque, Martin
    The current model of basal ganglia organization has been developed progressively over the last two decades in the light of key observations made at both experimental and clinical levels. This model has been highly successful in that it has stimulated a large amount of research in the field. However, several experimental and clinical findings that are at odds with the model have accumulated during the last decade. This paper reviews some of our own single-axon tracing studies in primates, which call for a re-evaluation of the current basal ganglia model.
  • PublicationRestreint
    Single-axon tracing study of corticostriatal projections arising from primary motor cortex in primates
    (Wistar Institute of Anatomy and Biology, 2006-03-14) Parent, Martin; Parent, André
    The axonal projections arising from the forelimb area of the primary motor cortex (M1) in cynomolgus monkeys (Macaca fascicularis) were studied following microiontophoretic injections of biotinylated dextran amine under electrophysiological guidance. The microinjections were centered on layer V, and 42 anterogradely labeled corticofugal axons were reconstructed from serial frontal or sagittal sections with a camera lucida. Our investigation shows that the primate striatum receives both direct and indirect projections from M1. The direct corticostriatal projection is formed by axons that remain uniformly thin and unbranched throughout their sinuous trajectory to the ipsilateral striatum. They divide as they enter the dorsolateral sector of the post-commissural putamen, the so-called sensorimotor striatal territory. The indirect corticostriatal projection derives from a thin collateral emitted within the corona radiata by thick, long-range fibers that descend toward the brainstem. The collateral enters the putamen dorsomedially and remains unbranched until it reaches the dorsolateral sector of the putamen, where it breaks out into two to four axonal branches displaying small and equally spaced varicosities. Both direct and indirect corticostriatal axons branch moderately but occupy vast rostrocaudal striatal territories, where they appear to contact en passant several widely distributed striatal neurons. These findings reveal that, in contrast to current beliefs, the primate motor corticostriatal system is not exclusively formed by axons dedicated solely to the striatum. It also comprises collaterals from long-range corticofugal axons, which can thus provide to the striatum a copy of the neural information that is being conveyed to the brainstem and/or spinal cord.
  • PublicationRestreint
    The microcircuitry of primate subthalamic nucleus
    (World Federation of Neurology, 2007-01-01) Parent, Martin; Parent, André
    Single-cell labeling experiments in cynomolgus monkeys have revealed that the subthalamic nucleus (STN) harbors several subtypes of projection neurons, each endowed with a highly patterned set of axon collaterals. This organizational feature allows single STN neurons to act directly upon the two major output structures of the basal ganglia--the substantia nigra pars reticulata and the internal pallidum--and, at the same time, to exert a multifarious effect upon the external pallidum with which the STN is reciprocally connected. These findings have clarified the role of the STN in basal ganglia organization and led to the elaboration of more accurate computational models of deep brain stimulation, a therapeutic approach currently used to alleviate the motor symptoms of Parkinson's Disease.
  • PublicationRestreint
    Two types of projection neurons in the internal pallidum of primates : single- axon tracing and three-dimensional reconstruction
    (Wistar Institute of Anatomy and Biology, 2001-09-28) Parent, Martin; Parent, André; Lévesque, Martin
    The axonal projections of the internal pallidum (GPi) in cynomolgus monkeys (Macaca fascicularis) were studied by labeling small pools of neurons with biotinylated dextran amine. Fifty-two axons were reconstructed entirely from serial sections with a camera lucida. Two types of projection neurons were identified in the GPi on the basis of their target sites. The abundant and centrally located type I neurons gave rise to a long axonal branch that descended directly to the pedunculopontine tegmental nucleus, where it arborized discretely. Other branches ascended to the thalamus and broke into 10-15 thinner collaterals that ran through most of the ventral anterior nucleus, where they terminated as typical plexuses. About half of these axons gave rise to collaterals that arborized in both components of the centre médian/parafascicular thalamic complex. The less numerous and peripherally located type II neurons had an axon that climbed the rostral thalamic pole, coursed along the stria medullaris, and arborized profusely within the lateral habenular nucleus, which stood out as the most densely innervated pallidal target. Some type II axons provided collaterals to the anterior thalamic nuclei. A small proportion of axons of both types had branches that crossed the midline and terminated in contralateral GPi target structures. Three-dimensional reconstruction showed that type I axons arborized principally along the sagittal plane. These data reveal that GPi neurons of type I act through a widely distributed axonal network upon thalamic and brainstem premotor neurons, whereas type II neurons act in a much more focused manner upon lateral habenular neurons.
  • PublicationRestreint
    Relationship between axonal collateralization and neuronal degeneration in basal ganglia
    (Springer-Verlag, 2006-01-01) Parent, Martin; Parent, André
    In this paper we evaluate the hypothesis of a possible link between the degree of axonal collateralization of neurons located within the different components of basal ganglia and the vulnerability of these neurons to neurodegenerative or neurotoxic events. Our results stemmed from single-cell labeling experiments in rodents and primates, immunohistochemical study of the dopaminergic nigrostriatal pathway in parkinsonian monkeys, and immunocytological analysis of the human striatum in normal individuals and in patients with Huntington’s disease. Our results indicate that projection neurons within virtually all basal ganglia components are endowed with a widespread and highly collateralized axon that yields a fixed number of terminals. Such a high degree of axonal collateralization allows exquisitely precise interactions between the various basal ganglia nuclei. However, the maintenance of this unique morphological trait implies high-energy consumption and renders basal ganglia neurons highly vulnerable to neurodegenerative, metabolic or neurotoxic insults.
  • PublicationAccès libre
    Axonal collateralization in primate basal ganglia and related thalamic nuclei
    (Cambridge University Press, 2002-12-01) Parent, Martin; Parent, André
    This paper provides an overview of the major organizational features of the basal ganglia and related thalamic centers, as delineated by the application of single-axon or single-cell labeling procedures in primates. These studies have revealed that the striatum, the external pallidum and the subthalamic nucleus harbor several types of projection neurons endowed with a highly collateralized axon that allows these neurons to interact with most components of the basal ganglia. In contrast, the internal pallidum, which is a major output structure of the basal ganglia, contains only two types of projection neurons. First, there is a minority of “limbic” pallidal neurons with a poorly branched axon that arborized profusely within the lateral habenula, which stands out as the most densely innervated pallidal target. Second, there is a majority of pallidal “motor” neurons with a long (total axonal length up to 27 cm) and highly branched axon that provides collaterals to the ventral tiers thalamic nuclei, the brainstem pedunculopontine nucleus and the centre médian/parafascicular thalamic complex. This type of axon allows internal pallidal neurons to send efferent copies of the same information to the thalamus and brainstem and hence influence various neuronal systems scattered throughout the neuraxis. Pallidal information is conveyed to the cerebral cortex and the striatum via the thalamus, while it is projected back to different components of the basal ganglia via the numerous reentrant pathways that arise from the pedunculopontine nucleus. Virtually all neurons in the centre médian thalamic nucleus innervate massively the striatum and less prominently the primary motor cortex, which in turn projects to the striatum directly or via a collateral from long-range corticofugal pyramidal axons. The results call for a reappraisal of our current concept of the anatomical and functional organization of basal ganglia, which play a crucial role in sensorimotor integration. Our data indicate that basal ganglia and related thalamic nuclei form a widely distributed neuronal network, whose elements are endowed with a highly patterned set of axon collaterals. This morphological feature allows a complex and exquisitely precise interaction between the various basal ganglia and related thalamic nuclei. The elucidation of this finely tuned network is needed to understand the complex spatiotemporal sequence of neural events that ensures the flow of cortical information through the basal ganglia and thalamus.
  • PublicationRestreint
    The pallidofugal motor fiber system in primates
    (World Federation of Neurology, 2004-04-13) Parent, Martin; Parent, André
    The organization of the pallidofugal fiber system originating from the internal segment of the globus pallidus (GPi) in cynomolgus monkeys (Macaca fascicularis) was studied by means of a single-axon tracing method. The primate GPi is composed of a majority of neurons endowed with a highly collateralized axon that projects to the premotor neurons located in the ventral tier thalamic nuclei, the center-médian/parafascicular thalamic complex and the brainstem pedunculopontine nucleus. These axons often follow a long and tortuous course within the GPi and then emerge either through the ansa lenticularis (AL) or the lenticular fasciculus (LF), irrespective of the location of their parent cell body in the GPi. Other pallidofugal axons exit through the medial pole of the GPi, at various distances between the AL ventrally and the LF dorsally. Virtually all pallidofugal axons course through Forel's field H, on their way to the thalamus and brainstem. They emit numerous short collaterals and boutons en passant in this sector of the subthalamic region, which stands out as a major target of GPi axons. Our results indicate that AL and LF do not form separate anatomical entities, each carrying axons originating from distinct functional pallidal territories, as commonly believed. Instead, these two fascicles form the ventral and dorsal borders of a morphological continuum that harbors a multitude of pallidofugal axons arising from all sectors of the GPi. This type of information should be taken into account when interpreting data from deep brain stimulation applied to pallidal and subthalamic regions in Parkinson's disease.