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Parent, André

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  • PublicationRestreint
    Asynaptic feature and heterogeneous distribution of the cholinergic innervation of the globus pallidus in primates
    (Springer Verlag, 2014-12-19) Parent, Martin; Eid, Lara; Parent, André
    The internal (GPi) and external (GPe) segments of the primate globus pallidus receive a significant cholinergic (ACh) innervation from the brainstem pedunculopontine tegmental nucleus. The present immunohistochemical study describes this innervation in the squirrel monkey (Saimiri sciureus), as visualized with an antibody raised against choline acetyltransferase (ChAT). At the light microscopic level, unbiased stereological quantification of ChAT positive (?) axon varicosities reveals a significantly lower density of innervation in GPi (0.26 ± 0.03 9 106) than in GPe (0.47 ± 0.07 9 106 varicosities/mm3 of tissue), with the anterior half of both segments more densely innervated than the posterior half. Neuronal density of GPi (3.00 ± 0.13 9 103 neurons/mm3) and GPe (3.62 ± 0.22 9 103 neurons/mm3) yields a mean ratio of ChAT? axon varicosities per pallidal neuron of 74 ± 10 in the GPi and 128 ± 28 in the GPe. At the electron microscopic level, the pallidal ChAT? axon varicosities are significantly smaller than their unlabeled counterparts, but are comparable in size and shape in the two pallidal segments. Only a minority of ChAT? varicosities displays a synaptic specialization (12 % in the GPi and 17 % in the GPe); these scarce synaptic contacts are mostly of the symmetrical type and occur exclusively on pallidal dendrites. No ChAT? axo-axonic synaptic modulatory action on pallidal afferents through diffuse transmission, whereas pallidal neurons may be influenced by both volumic and synaptic delivery of ACh.
  • PublicationAccès libre
    Evidence for sprouting of dopamine and serotonin axons in the pallidum of Parkinsonian monkeys
    (Frontiers Research Foundation, 2018-05-15) Gagnon, Dave; Whissel, Carl; Di Paolo, Thérèse; Parent, Martin; Eid, Lara; Parent, André; Coudé, Dymka
    This light and electron microscopie immunohistochemical quantitative study aimed at determining the state of the dopamine (DA) and serotonin (5-HT) innervations of the internal (GPi) and external (GPe) segments of the pallidum in cynomolgus monkeys (Macaca fascicularis) rendered parkinsonian by systemic injections of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). In contrast to the prominent DA denervation of striatum, the GPi in MPTP monkeys was found to be markedly enriched in DA (TH+) axon varicosities. The posterior sensorimotor region of this major output structure of the basal ganglia was about 8 times more intensely innervated in MPTP monkeys (0.71 ± 0.08 × 106 TH+ axon varicosities/mm3) than in controls (0.09 ± 0.01 × 106). MPTP intoxication also induced a two-fold increase in the density of 5-HT (SERT+) axon varicosities in both GPe and GPi. This augmentation was particularly pronounced anteriorly in the so-called associative and limbic pallidal territories. The total length of the labeled pallidal axons was also significantly increased in MPTP monkeys compared to controls, but the number of DA and 5-HT axon varicosities per axon length unit remained the same in the two groups, indicating that the DA and 5-HT pallidal hyperinnervations seen in MPTP monkeys result from axon sprouting rather than from the appearance of newly formed axon varicosities on non-growing axons. At the ultrastructural level, pallidal TH+ and SERT+ axons were morphologically similar in MPTP and controls, and their synaptic incidence was very low suggesting a volumic mode of transmission. Altogether, our data reveal a significant sprouting of DA and 5-HT pallidal afferents in parkinsonian monkeys, the functional significance of which remains to be determined. We suggest that the marked DA hyperinnervation of the GPi represents a neuroadaptive change designed to normalize pallidal firing patterns associated with the delayed appearance of motor symptoms, whereas the 5-HT hyperinnervation might be involved in the early expression of non-motor symptoms in Parkinson's disease.
  • PublicationRestreint
    The Primate basal ganglia connectome as revealed by single-axon tracing
    (Elsevier, 2015-12-01) Parent, Martin; Parent, André
    This chapter provides an overview of the basal ganglia connectome as revealed by single-axon tracing procedures applied to nonhuman primates. These studies have shown that virtually all basal ganglia components, as well as most brainstem and thalamic nuclei with which they are reciprocally linked, harbor several distinct sets of projection neurons characteristically endowed with a highly collateralized and widely distributed axon. This morphological trait allows a complex and exquisitely precise interaction between the various basal ganglia and their related thalamic and brainstem nuclei. Our findings indicate that the basal ganglia are part of a finely tuned network that extends over several levels of the neuraxis. The anatomical elucidation of this intricate circuitry is essential to understand the complex spatiotemporal sequence of neural events that ensures the flow of cortical information through the basal ganglia, whose alteration leads to major psychomotor disabilities.
  • 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
    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
    The number of striatal cholinergic interneurons expressing calretinin is increased in parkinsonian monkeys
    (Blackwell Science, 2016-07-05) Di Paolo, Thérèse; Parent, Martin; Petryszyn, Sarah; Parent, André
    The most abundant interneurons in the primate striatum are those expressing the calcium-binding protein calretinin (CR). The present immunohistochemical study provides detailed assessments of their morphological traits, number, and topographical distribution in normal monkeys (Macaca fascicularis) and in monkeys rendered parkinsonian (PD) by MPTP intoxication. In primates, the CR + striatal interneurons comprise small (8–12 μm), medium (12–20 μm) and large-sized (20–45 μm) neurons, each with distinctive morphologies. The small CR + neurons were 2–3 times more abundant than the medium-sized CR + neurons, which were 20–40 times more numerous than the large CR + neurons. In normal and PD monkeys, the density of small and medium-sized CR + neurons was twice as high in the caudate nucleus than in the putamen, whereas the inverse occurred for the large CR + neurons. Double immunostaining experiments revealed that only the large-sized CR + neurons expressed choline acetyltransferase (ChAT). The number of large CR + neurons was found to increase markedly (4–12 times) along the entire anteroposterior extent of both the caudate nucleus and putamen of PD monkeys compared to controls. Comparison of the number of large CR −/ChAT + and CR +/ChAT + neurons together with experiments involving the use of bromo-deoxyuridine (BrdU) as a marker of newly generated cells showed that it is the expression of CR by the large ChAT + striatal interneurons, and not their absolute number, that is increased in the dopamine-depleted striatum. These findings reveal the modulatory role of dopamine in the phenotypic expression of the large cholinergic striatal neurons, which are known to play a crucial role in PD pathophysiology.
  • 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 calretinin interneurons of the striatum : comparisons between rodents and primates under normal and pathological conditions
    (Springer-Verlag, 2017-02-06) Parent, Martin; Petryszyn, Sarah; Parent, André
    This paper reviews the major organizational features of calretinin interneurons in the dorsal striatum of rodents and primates, with some insights on the state of these neurons in Parkinson’s disease and Huntington’s chorea. The rat striatum harbors medium-sized calretininimmunoreactive (CR?) interneurons, whereas the mouse striatum is pervaded by medium-sized CR? interneurons together with numerous small and highly immunoreactive CR? cells. The CR interneuronal network is even more elaborated in monkey and human striatum where, in addition to the small- and medium-sized CR? interneurons, a set of large CR? interneurons occurs. The majority of these giant CR? interneurons, which are unique to the primate striatum, also display immunoreactivity for choline acetyltransferase (ChAT), a faithful marker of cholinergic neurons. The expression of CR and/or ChAT by the large striatal interneurons appears to be seriously compromised in Parkinson’s disease and Huntington’s chorea. The species differences noted above have to be considered to better understand the role of CR interneurons in striatal organization in both normal and pathological conditions.
  • 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.