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Jeff Paré


I am the day-to-day supervisor of Yoland's lab. I have been working with Yoland since 1992. I believe I was the first employee of his lab when he started his career as independent scientist in the early 1990's. I obtained a Laboratory Technologist diploma from Ste-Foy College, Québec, Canada in 1989. I worked in the Departments of Biochemistry and Pathology in different hospitals in Québec before moving to Atlanta with Yoland's lab in 1996.

Although my main responsibility is to assume the day-to-day running of the lab and train new members of the laboratory in the use of different techniques and equipment, I also spend a great deal of energy developing and refining new techniques.

As my role in the lab evolved, I started working on different research projects. The most important one I am currently involved in deals with the synaptology and chemistry of inputs to thalamostriatal neurons in primates. The existence of a brainstem cholinergic input to the thalamus from the pedunculopontine tegmental nucleus (PPN) has been long known, but the heterogeneity of neurotransmitters used by this projection has never been studied in great detail. Using double and triple electron microscopic immunocytochemical procedures, we have found that the content of neurotransmitter by this ascending cholinergic pathway differs between inputs that terminate in th erelay sensory versus caudal intralaminar nuclei. We were able to demonstrate that some of the terminals that innervate the intralaminar nuclei contain acetylcholine or acetylcholine with GABA or glutamate. Furthermore, we also showed that a significant proportion of boutons contained the three neurotransmitters (i.e. GABA, glutamate and acetylcholine).

The significance of such findings is still unknown, but one could wonder how complex and multifarious the effects of these projections may be on the neuronal activity in the primate thalamus.

 

photo fo jeff working at the confocal microscopePUBLICATIONS

Peer-reviewed manuscripts:

 

Mitrano, D.A., J.-F. Pare and Y. Smith (2010) Ultrastructural relationships between cortical, thalamic and amygdala glutamatergic inputs and group I metabotropic glutamate receptors in the rat accumbens. J. Comp. Neurol. 518: 1315-1329. PMID. 20151362.

Lee, H., HL Melrose, JF Pare, MJ Farrer and Y Smith (2010) Lrrk2 localization in the primate basal ganglia and thalamus: A light and electron microscopic analysis in monkeys. Exptl Neurology 224: 438-447. PMID. 20483355.

Newell-Litwa, K., S. Chintala, S. Jenkins, J.-F. Pare, L. McGaha, Y.Smith and V. Faundez (2010) Hermansky-Pudlak protein complexes, AP-3 and BLOC-1, differentially regulate presynaptic composition in the striatum and hippocampus. J.Neurosci. 30: 820-831. PMID. 20089890.

Kliem, M., J-F Pare, Z.Khan, T.Wichmann and Y. Smith (2010) Ultrastructural localization of dopamine D1-like receptors in the substantia nigra pars reticulate and the internal segment of the globus pallidus in parkinsonian monkeys. Eur. J. Neurosci. 31: 836-851. PMID. 20374284.

Smith, Y, D. Raju, B Nanda, JF Pare, A Galvan and T Wichmann (2009) The thalamostriatal systems: Anatomical and functional organization in normal and parkinsonian states. Brain res Bull 78:60-68, PMID: 18805468.

Kleim, MA, JF Pare, ZU Khan, T, Wichmann and Y. Smith (2009) Comparative ultrastructure analysis of D1 and D5 dopamine receptor distribution in the substantia nigra and globus pallidus of monkeys. Adv. Behav. Biol. 58: 239-253. PMID 19750130.

Mitrano, DA, JF Pare and Y Smith (2009) Ultrastructural relationships between cortical, thalamic, and amygdala glutamatergic inputs and group I metabotropic glutamate receptors in the rat accumbens, J. Comp. Neurol.

Lee, H, HL Melrose, JF PAre, MJ Farrer and Y Smith (2009) Lrrk2 localization in the primate basalganglia and Comp. Neurol.

Tippen, AL, JF Pare, N Langwieser, S Moosmang, T Milner, Y Smith and A Lee(2008) Ultrastructural evidence for pre and postsynaptic localization of Cav1.2 L-Type Ca2+ channels in the rat hippocampus. J Comp Neurol 506: 569-583.

Elfenbein, HA, RF Rosen, SL Stephens, RC Switzer, Y Smith, J Pare, R Warzok and L Walker (2007) Cerebral b -amyloid angiopathy in aged squirrel monkeys.

Smith, Y, D. Raju and JF Pare (2007) Functional anatomy and synaptic circuitry of the thalamostriatal systems. Brain Res. Bull.

Tippen, AL, JF Pare, N Langwieser, S Moosmang, TA Milner, Y Smith and A. Lee (2007) Ultrastructural evidence for pre- and post-synaptic localization of Cav 1.2 L-type Ca+2 channels in the rat hippocampus. J. Comp. Neurol.

JF Pare, N Langwieser, S Moosmang, TA Milner, Y Smith and A. Lee (2007) Ultrastructural evidence for pre- and post-synaptic localization of Cav 1.2 L-type Ca+2 channels in the rat hippocampus. J. Comp. Neurol.

Bough, KJ, M Paquet, JF Pare, B Hassel, Y Smith, RA Hall and R Dingledine (2007) Evidence against enhanced glutamate transport in the anticonvulsant mechanism of the ketogenic diet. Epilepsy Res. 74: 232-236

Bough, KJ, J Wetherington, B Hassel, JF Pare, J Gawryluk, JG Greene, R Shaw, Y Smith, JD Geiger and RJ Dingledine (2006) Mitochondrial biogenesis induced by ketogenic diet in rat hippocampus. Ann. Neurol 60: 223-235.

Charara, A, J.-F. Pare, A.I. Levey and Y. Smith (2005) Synaptic and extrasynaptic GABA-A and GABA-B receptors in the globus pallidus: An electron microscopic immunogold analysis in monkeys. Neuroscience 131: 917-933.

J.-F. Pare, A.I. Levey and Y. Smith (2005) Synaptic and extrasynaptic GABA-A and GABA-B receptors in the globus pallidus: An electron microscopic immunogold analysis in monkeys. Neuroscience 131: 917-933.

Galvan, A., A. Charara, J.-F. Pare, J.M. Fritschy, A.I. Levey and Y. Smith (2004) Differential subsynaptic llocalization of GABA-A and GABA-B receptors in the primate subthalamic nucleus. Neuroscience (in press).

Smith, Y. , D. Raju, J.-F. Pare and M. Sidibe (2004) The thalamostriatal system: A highly specific network of the basal ganglia circuitry. Trends in Neurosci. 27: 520-527.

Sidibe, M., Pare, J-F., Raju, D and Smith Y. (2003) Anatomical and functional relationships between intralaminar thalamic nuclei and basal ganglia in monkeys. In L.F.B. Nicholson and R.L.M. Faull (eds), The Basal Ganglia VII, pp. 409-420, Plenum Publishers: New York.

Sidibe, M., J.-F. Pare and Y. Smith (2002) Anatomical and functional relationships between intralaminar thalamic nuclei and basal ganglia in monkeys. In Faull, R.L.M. and Nicholson, L. (eds) “Basal Ganglia VII”. Plenum Press: New York, pp. 233-242.

J.-F. Pare and Y. Smith (2002) Anatomical and functional relationships between intralaminar thalamic nuclei and basal ganglia in monkeys. In Faull, R.L.M. and Nicholson, L. (eds) “Basal Ganglia VII”. Plenum Press: New York, pp. 233-242.

Smith, Y., Charara, A., Paquet, M., Kieval, J., Pare, J-F., Hanson, J., Hubert, G.H., Kuwajima, M. and Levey, A. (2001). Ionotropic and metabotropic GABA and glutamate receptor in primate basal ganglia. J. of Chemical Neuroanatomy 22: 13-42

Sidibe, M., Paré, J.-F., Smith, Y. (2001). Nigral and Pallidal inputs to functionally segregated thalamostriatal neurons in the centromedian/parafascicular intralaminar nuclear complex in monkeys. J. of Comp. Neurol. 447: 286-299

Kieval, J.Z., Paré, J.-F., Charara, A., Smith, Y. (2001). Subcellular and subsynaptic localization of kainate receptors subunits in the monkey striatum. J. Neurosci. 21(22): 8746-8757

Smith Y., Paré J.-F., Paré D. (2000). Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J. of Comparative Neurology 416(4):496-508

Smith Y., Paré J.-F., Paré D. (1998). The intra-amygdaloid network: Ultrastructural organization of parvalbumin-immunoreactive elements. J. of Comparative Neurology 391: 164-179.

Paré D., Smith Y., Paré J.-F. (1995). Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat: Phaseolous vulgaris-leucoagglutinin anterograde tracing at the light and electron microscopic level. Neuroscience 69, 567-583.

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confocal image

This image, acquired at the confocal microscope, shows TH-positive neurons (green) and mGluR5-positive elements (red) in the Substancia Nigra pars compacta of the monkey. Colocalization of TH and mGluR5 elements are displayed in yellow. Note that only the proximal dendrites in the field are colocalized.


Abstracts:

Gonzales, KK, JF Pare, S Jenkins, T Wichmann and Y Smith (2010) Striatal cholinergic interneurons receive intrinsic GABAergic inputs from axon collaterals of direct and indirect striatofugal neurons in the primate putamen. IBAGS X Abstr P-61.

Mathai, A., JF Pare, S Jenkins and Y. Smith (2010) Glutamatergic inputs to the subthalamic nucleus: A quantitative analysis of the synaptic microcircuitry of vGluT1- and vGluT2-containing terminals in normal and parkinsonian nonhuman primates. IBAGS X Abstr P-28.

Gonzales KK, JF Pare, S Jenkins, T Wichmann and Y Smith (2009) Intrinsic microcircuitry of GABAergic inputs from direct and indirect striatofugal neurons on striatal cholinergic interneurons in the primate putamen. Soc for Neurosci Abstr 828.4

Mathai, A, JF Pare, S Jenkins, Y Smith (2009) Glutamatergic inputs to the subthalamic nucleus: A quantitative analysis of the synaptic microcircuitry of vGluT1- and vGluT2-containing terminals in nonhuman primates. Soc for Neurosci Abstr 828.2.

Bogenpohl J, J Pare, Y Smith (2008) Subcellular localization of the adenosine A2A receptor in the monkey basal ganglia. Soc Neurosci Abstr 825.23.

Boghenpohl JW, Pare JF and Smith Y (2007) Subcellular localization of adenosine A2A receptors in the striatum and globus pallidus of monkey and rat. IBAGS IXth Proceedings, Abstr P-056, p. 93

Kliem MA, Pare J, Maxson S, Wichmann T, Smith Y (2006) Comparative ultrastructural analysis of D1 and D5 dopamine receptor distribution in the substantia nigra and globus pallidus of normal and parknsonian monkeys. Soc for Neurosci Abstr 450.12

Tippens AL, Pare J, Smith Y, Lee A (2006) Postsynaptic localization of caldendrin, a neuronal Ca+2-binding protein, and Cav1.2 (L-type) Ca+2 channels in rat hippocampus. Soc for Neurosci abstr 340.4.

Pare, J-F, DV Raju and Y. Smith (2005) Axonal tract tracing: A historical survey of neuroanatomical tract tracing methods. Soc for Neurosci abstr 18.19

Smith, Y and J-F Pare (2004) Differential co-localization of GABA and glutamate in ascending brainstem cholinergic inputs tobasal ganglia in monkeys. 8th IBAGS meeting, Crieff, P45

Raju, DV,J Pare and Y Smith (2004) A subset of cholinergic terminals co-express the vesicular glutamate transporter 1 in the monkey striatum. Soc for NS abstr 307.2

Pare, J-F, Y Smith (2004) Acetylcholine co-localizes with GABA or glutamate in ascending brainstem inputs to the substantia nigra/ventral tegmental area and subthalamic nucleus in monkey. Soc for NS abstr 307.1

Pare, J.-F., Sidibe, M and Smith, Y. (2003). Co-existence of GABA and Acetylcholine in Pedunculopontine tegmental inputs in intralaminar nuclei, but not sensory relay nuclei in monkey thalamus. Soc. For NS meeting abstr 246.12

Mitrano, D.A., Paré, J.-F. and Smith, Y. (2003). Subcellular and subsynaptic localization of mGluR5 in the shell and core of the nucleus accumbens in the Rhesus monkey. Soc. For NS meeting abstr 800.3

Iskhakova, L.A., M. Paquet, J.-F. Pare and Y. Smith (2002) Subcellular localization of group II metabotropic glutamate receptors in the monkey striatum. Soc. For NS meeting abstr 63.3.

Sidibe, M., J.-F. Pare and Y. Smith (2002) Subcellular and subsynaptic localization of GABA-A alpha 1 and GABA-BR1 receptors subunits in the ventral motor and centromedian/ parafascicular (CM/Pf) thalamic nuclei in monkeys. Soc for NS meeting abstr 460.11.

Felger, J., J.-F. Pare, Y. Smith, Plotsky, PM and M. Sanchez (2002) Localization of glococorticoid receptors to presynaptic elements containing both GABA and glutamate in the primate hippocampus. Soc for NS meeting abstr. 28: 470.15.

Smith, Y., Betarbet, R., Pare, J.-F. and Greenamyre JT (2002) Subcellular localization of GluR1 AMPA glutamate receptor subunit in the striatum of normal
and parkinsonian monkeys. Soc for NS meeting abstr 788.3.

Pare, J.-F., R. Samson, Y. Smith and D. Pare (2002) Transverse processing modules in the lateral nucleus of the amygdala. Soc for ns meeting abstr 28:587.7

Kuwajima, M., K.B. Philpot, J.-F. Pare and Y. Smith (2001) Subcellular localization
of group I metabotropic glutamate receptors in the monkey subthalamic nucleus. Soc. for Neurosci. 27: 290.12

Sidibe, M., J.-F. Pare and Y. Smith (2001) Co-localization of GABA and choline acetyltransferase in pedunculopontine projections to the centre median/parafascicular (CM/PF) nuclei in monkeys.
Soc. for Neurosci. 27: 290.15.

Smith, Y., J.-F. Pare and A. Charara (2001) Subsynaptic localization of GABA-A and GABA-B receptors in the monkey globus pallidus. Soc. for Neurosci. 27: 290.11.

Smith, Y., M. Sidibe and J.-F. Pare and D. Raju (2001) Anatomical and functional relationships between intralaminar thalamic nuclei and basal ganglia in monkeys.Proc. VIIth IBAGS meeting, New Zealand

Galvan, A., A. Charara, J.-F. Pare, A.I. Levey, J.-M. Fritschy and Y. Smith (2001) Differential subcellular and subsynaptic distribution of GABA-B and GABA-A receptors in the subthalamic nucleus. Soc. for Neurosci. 27: 290.10.

Sanchez, M.M., A. Charara, J.-F. Paré, Y. Smith and P.M. Plotsky (2000) Pre- and post-synaptic localization of glucocorticoid receptors in the primate hippocampal formation. Soc. For Neurosci. 26: 152.5.

Martina, M., S. Royer, J.-F. Paré, Y. Smith and D. Paré (2000) Perirhinal propagation of neocortical inputs. Soc. for Neurosci. 26: 172.14.

Smith, Y., M. Sidibé and J.-F. Paré (2000) Synaptic inputs from the substantianigra and the pedunculopontine nucleus to thalamostriatal neurons. Soc. for Neurosci. 26: 361.15.

Kieval, J.Z., A. Charara, J.-F. Paré and Y. Smith (2000) Subcellular localization of kainate receptors in the monkey striatum. Soc. for Neurosci. 26: 741.15.

Paré, J.-F., A. Charara and Y. Smith (1999) High pressure freezing and freeze substitution as tools for post-embedding immunocytochemistry in monkey brain sections. Microsc. Microanal., Vol. 5: 1300.

Dall Vechia, S.E., J.-F. Paré, P. Lambert, P. Couceyro, M. Kuhar and Y. Smith (1998) CART peptide immunoreactivity in the hypothalamic PVN in monkeys: Distribution and interactions with NPY. CPDD abstr. 60: 179.

Also acquired at the confocal microscope, this image shows TH-positive neurons (green), mGluR5-positive elements (red) and VGLuT-1 (blue) in the Substancia Nigra pars compacta of the monkey. Colocalization of TH and mGluR5 elements are again, the elements displayed in yellow whereas colocalization of the TH, mGluR5 and VGLuT-1 elements are shown in purple.

confocal image

Paré, J.-F., S.E. Dall Vechia, P. Lambert, P. Couceyro, B.E. Garrett, M. Kuhar and Y. Smith (1998) CART peptide-immunoreactive neurons in the monkey PVN: Electron microscopic characterization and synaptic relationships with NPY-immunoreactive terminals. Soc. for Neurosci. 24: 817.4.

Dall Vechia, S.E., J.-F. Paré, P. Lambert, P. Couceyro, M. Kuhar and Y. Smith (1998) Synaptic interactions between CART peptide-immunoreactive terminals and midbrain dopaminergic neurons in the rat. Soc. for Neurosci. 24: 817.3.

Hubert, G.W., J.-F. Paré, A.M. Robida, S.R. Bradley, A.I. Levey, P.J. Conn and Y. Smith (1998) Subsynaptic localization of metabotropic glutamate receptors (mGluRs) in the globus pallidus and subthalamic nucleus in monkeys. Soc. for Neurosci. 24: 648.14.

Kieval, J.Z., J.-F. Paré, P. Couceyro, M.J. Kuhar and Y. Smith (1998) Electron microscopic characterization of CART peptide-immunoreactive neurones in the nucleus accumbens in monkeys. Proceedings 6th International Basal Ganglia Society Meeting, Brewster, MA, p. 62.

Dall Vechia, S.E., J.-F. Paré, P. Lambert, P. Couceyro, M.J. Kuhar and Y. Smith (1998) Electron microscopic characterization of CART peptide-immunoreactive terminals in the substantia nigra compacta in rats. Proceedings 6th International Basal Ganglia Society Meeting, Brewster, MA, p. 62.

Smith, Y., G.W. Hubert, J.E. Hanson, J.-F. Paré, S.R. Bradley, P.J. Conn and A.I.Levey (1998) Subsynaptic localization of metabotropic glutamate receptors in the basal ganglia in monkeys: II. Globus pallidus and subthalamic nucleus. Proceedings 6th International Basal Ganglia Society Meeting, Brewster, MA, p. 12.

Paré, J.-F., Y. Smith, D. Paré and M. Filion (1997) Cortical inputs to inhibitory interneurons of the basolateral (BL) amygdaloid complex. Soc. for Neurosci. 23: 817.7

Freedman, L., J.-F. Paré, T.R. Insel and Y. Smith (1997) Subcortical projections of macaque infralimbic cortex (area 25). Soc. for Neurosci. 23: 359.4.

Smith, Y., J.-F. Paré, E. Koylu, P. Couceyro, E. Ince, A.I. Levey and M.H. Kuhar (1997) CART peptide immunoreactivity in the nucleus accumbens of monkeys: Electron microscopic analysis and co-localization studies. Soc. for Neurosci. 23: 384.6.

Thomas, T.M., J.-F. Paré, Y. Smith and S. Hersch (1997) Analysis of frontal cortical inputs to striatal cholinergic interneurons in monkey. Soc. for Neurosci. 23: 82.4.

Paré, J.-F., Y. Smith and D. Paré (1996) Synaptic organization of parvalbumin-immunoreactive neurones in the lateral and basolateral amygdaloid nuclei in the cat. Soc. for Neurosci. 22: 806.9.

Paré, D., Y. Smith and J.-F. Paré (1995) Intrathalamic projections of the intralaminar nuclei (ITN): Possible anatomical substrate of large-scale thalamocortical synchronization. Soc. for Neurosci. 21: 112.

Paré, D., Y. Smith and J.-F. Paré (1993) GABAergic projections from the intercalated cell masses (ICMs) to the centromedial (CM) amygdaloid complex
and basal forebrain (BF). Soc. for Neurosci. 19: 1440.

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