Subpopulations of cholinergic, GABAergic and glutamatergic neurons in the pedunculopontine nucleus contain calcium-binding proteins and are heterogeneously distributed

European Journal of Neuroscience

Volumn 35, Issue 5, 2012, Pages 723-734

  Martinez Gonzalez, Cristina ^a   Wang, Hui Ling ^b   Micklem, Benjamin R ^a   Bolam, J Paul ^a   Mena Segovia, Juan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Brainstem; Calbindin; Calretinin; In situ hybridization; Rat; Stereology

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALBINDIN; CALRETININ; CHOLINE ACETYLTRANSFERASE; MESSENGER RNA; PARVALBUMIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALBINDIN GENE; CALRETININ GENE; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE; CONTROLLED STUDY; DNA DETERMINATION; GABAERGIC SYSTEM; GAD GENE; GENE; GENE EXPRESSION; GENE SEQUENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; VGLUT2 GENE;

ANIMALS; CALCIUM-BINDING PROTEINS; CHOLINERGIC NEURONS; GABAERGIC NEURONS; GLUTAMIC ACID; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84862831131     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08002.x     Document Type: Article

References (49)

1. Acsady, L., Halasy, K. & Freund, T.F. (1993) Calretinin is present in non-pyramidal cells of the rat hippocampus - III. Their inputs from the median raphe and medial septal nuclei. Neuroscience, 52, 829-841.
2. Alderson, H.L., Latimer, M.P. & Winn, P. (2006) Intravenous self-administration of nicotine is altered by lesions of the posterior, but not anterior, pedunculopontine tegmental nucleus. Eur. J. Neurosci., 23, 2169-2175.
3. Alderson, H.L., Latimer, M.P. & Winn, P. (2008) A functional dissociation of the anterior and posterior pedunculopontine tegmental nucleus: excitotoxic lesions have differential effects on locomotion and the response to nicotine. Brain Struct. Funct., 213, 247-253.
4. Beninato, M. & Spencer, R.F. (1986) A cholinergic projection to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry. J. Comp. Neurol., 253, 525-538.
5. Boucetta, S. & Jones, B.E. (2009) Activity profiles of cholinergic and intermingled GABAergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-anesthetized rats. J. Neurosci., 29, 4664-4674.
6. Camp, A.J. & Wijesinghe, R. (2009) Calretinin: modulator of neuronal excitability. Int. J. Biochem. Cell Biol., 41, 2118-2121.
7. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35, 375-475.
8. Charara, A. & Parent, A. (1994) Brainstem dopaminergic, cholinergic and serotoninergic afferents to the pallidum in the squirrel monkey. Brain Res., 640, 155-170.
9. Chard, P.S., Bleakman, D., Christakos, S., Fullmer, C.S. & Miller, R.J. (1993) Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J. Physiol., 472, 341-357.
10. Clements, J.R. & Grant, S. (1990) Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci. Lett., 120, 70-73.
11. Coté, P.Y. & Parent, A. (1992) Calbindin D-28k and choline acetyltransferase are expressed by different neuronal populations in pedunculopontine nucleus but not in nucleus basalis in squirrel monkeys. Brain Res., 593, 245-252.
12. Dun, N.J., Dun, S.L., Hwang, L.L. & Forstermann, U. (1995) Infrequent co-existence of nitric oxide synthase and parvalbumin, calbindin and calretinin immunoreactivity in rat pontine neurons. Neurosci. Lett., 191, 165-168.
13. Ford, B., Holmes, C.J., Mainville, L. & Jones, B.E. (1995) GABAergic neurons in the rat pontomesencephalic tegmentum: codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J. Comp. Neurol., 363, 177-196.
14. Fortin, M. & Parent, A. (1999) Calretinin-immunoreactive neurons in primate pedunculopontine and laterodorsal tegmental nuclei. Neuroscience, 88, 535-547.
15. Garcia-Rill, E., Houser, C.R., Skinner, R.D., Smith, W. & Woodward, D.J. (1987) Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus. Brain Res. Bull., 18, 731-738.
16. Garcia-Rill, E., Kinjo, N., Atsuta, Y., Ishikawa, Y., Webber, M. & Skinner, R.D. (1990) Posterior midbrain-induced locomotion. Brain Res. Bull., 24, 499-508.
17. Gritti, I., Manns, I.D., Mainville, L. & Jones, B.E. (2003) Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J. Comp. Neurol., 458, 11-31.
18. Gulyas, A.I., Toth, K., Danos, P. & Freund, T.F. (1991) Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28k, and cholecystokinin in the rat hippocampus. J. Comp. Neurol., 312, 371-378.
19. Inglis, W.L., Olmstead, M.C. & Robbins, T.W. (2001) Selective deficits in attentional performance on the 5-choice serial reaction time task following pedunculopontine tegmental nucleus lesions. Behav. Brain Res., 123, 117-131.
20. Kita, T. & Kita, H. (2010) Cholinergic and non-cholinergic mesopontine tegmental neurons projecting to the subthalamic nucleus in the rat. Eur. J. Neurosci., 33, 433-443.
21. Kretsinger, R.H. & Nockolds, C.E. (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J. Biol. Chem., 248, 3313-3326.
22. Lavoie, B. & Parent, A. (1994) Pedunculopontine nucleus in the squirrel monkey: projections to the basal ganglia as revealed by anterograde tract-tracing methods. J. Comp. Neurol., 344, 210-231.
23. Martinez-Gonzalez, C., Bolam, J.P. & Mena-Segovia, J. (2011) Topographical organization of the pedunculopontine nucleus. Front. Neuroanat., 5, 22-31.
24. Matsumura, M., Nambu, A., Yamaji, Y., Watanabe, K., Imai, H., Inase, M., Tokuno, H. & Takada, M. (2000) Organization of somatic motor inputs from the frontal lobe to the pedunculopontine tegmental nucleus in the macaque monkey. Neuroscience, 98, 97-110.
25. Mena-Segovia, J., Sims, H.M., Magill, P.J. & Bolam, J.P. (2008a) Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J. Physiol., 586, 2947-2960.
26. Mena-Segovia, J., Winn, P. & Bolam, J.P. (2008b) Cholinergic modulation of midbrain dopaminergic systems. Brain Res. Rev., 58, 265-271.
27. Mena-Segovia, J., Micklem, B.R., Nair-Roberts, R.G., Ungless, M.A. & Bolam, J.P. (2009) GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J. Comp. Neurol., 515, 397-408.
28. Mesulam, M.M., Mufson, E.J., Wainer, B.H. & Levey, A.I. (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience, 10, 1185-1201.
29. Motts, S.D. & Schofield, B.R. (2009) Sources of cholinergic input to the inferior colliculus. Neuroscience, 160, 103-114.
30. 2+. Biophys. J., 79, 3009-3018.
31. Oakman, S.A., Faris, P.L., Kerr, P.E., Cozzari, C. & Hartman, B.K. (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J. Neurosci., 15, 5859-5869.
32. Olszewski, J. & Baxter, D. (1982) Cytoarchitecture of the Human Brain Stem. S. Karger AG, Basel.
33. Pahapill, P.A. & Lozano, A.M. (2000) The pedunculopontine nucleus and Parkinson's disease. Brain, 123, 1767-1783.
34. Parent, A., Fortin, M., Coté, P.Y. & Cicchetti, F. (1996) Calcium-binding proteins in primate basal ganglia. Neurosci. Res., 25, 309-334.
35. Pochet, R., Parmentier, M., Lawson, D.E. & Pasteels, J.L. (1985) Rat brain synthesizes two 'vitamin D-dependent' calcium-binding proteins. Brain Res., 345, 251-256.
36. Ros, H., Magill, P.J., Moss, J., Bolam, J.P. & Mena-Segovia, J. (2010) Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states. Neuroscience, 170, 78-91.
37. Saitoh, K., Hattori, S., Song, W.J., Isa, T. & Takakusaki, K. (2003) Nigral GABAergic inhibition upon cholinergic neurons in the rat pedunculopontine tegmental nucleus. Eur. J. Neurosci., 18, 879-886.
38. Schwaller, B., Meyer, M. & Schiffmann, S. (2002) 'New' functions for 'old' proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum, 1, 241-258.
39. Skinner, R.D. & Garcia-Rill, E. (1984) The mesencephalic locomotor region (MLR) in the rat. Brain Res., 323, 385-389.
40. Smith, Y., Pare, D., Deschenes, M., Parent, A. & Steriade, M. (1988) Cholinergic and non-cholinergic projections from the upper brainstem core to the visual thalamus in the cat. Exp. Brain Res., 70, 166-180.
41. Staiger, J.F., Masanneck, C., Schleicher, A. & Zuschratter, W. (2004) Calbindin-containing interneurons are a target for VIP-immunoreactive synapses in rat primary somatosensory cortex. J. Comp. Neurol., 468, 179-189.
42. Steininger, T.L., Wainer, B.H., Blakely, R.D. & Rye, D.B. (1997) Serotonergic dorsal raphe nucleus projections to the cholinergic and noncholinergic neurons of the pedunculopontine tegmental region: a light and electron microscopic anterograde tracing and immunohistochemical study. J. Comp. Neurol., 382, 302-322.
43. Steriade, M., Pare, D., Parent, A. & Smith, Y. (1988) Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey. Neuroscience, 25, 47-67.
44. Steriade, M., Datta, S., Pare, D., Oakson, G. & Curro Dossi, R.C. (1990) Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J. Neurosci., 10, 2541-2559.
45. Vincent, S.R. & Kimura, H. (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience, 46, 755-784.
46. Vincent, S.R., Satoh, K., Armstrong, D.M. & Fibiger, H.C. (1983) NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci. Lett., 43, 31-36.
47. Wang, H.L. & Morales, M. (2008) Corticotropin-releasing factor binding protein within the ventral tegmental area is expressed in a subset of dopaminergic neurons. J. Comp. Neurol., 509, 302-318.
48. Wang, H.L. & Morales, M. (2009) Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur. J. Neurosci., 29, 340-358.
49. Winn, P. (2008) Experimental studies of pedunculopontine functions: are they motor, sensory or integrative? Parkinsonism Relat. Disord., 14(Suppl 2), S194-S198.