The ventrolateral upper cervical cell group in cat projects to all rostrocaudal levels of the periaqueductal gray matter

Brain Research

Volumn 1300, Issue , 2009, Pages 79-96

  Mouton, Leonora J ^a   Eggens Meijer, Ellie ^a   Klop, Esther Marije ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Neck muscle; Somatosensory; Spinomesencephalic; Spinothalamic; Vestibular; Visceral

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN STEM; CAT; CELL; CELL FUNCTION; CELL NUCLEUS; CERVICAL SPINAL CORD; CONTROLLED STUDY; MESENCEPHALON; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; SENSORY NERVE; SOMATIC CELL; SPINAL CORD; SPINAL CORD VENTRAL HORN; THALAMUS; VENTROLATERAL UPPER CERVICAL CELL; VESTIBULAR STIMULATION; ANIMAL; ANTERIOR HORN CELL; CERVICAL SPINE; NERVE TRACT; PHYSIOLOGY;

RATTUS;

TRACER;

ANIMALS; ANTERIOR HORN CELLS; CATS; CERVICAL VERTEBRAE; NEURAL PATHWAYS; NEURONAL TRACT-TRACERS; PERIAQUEDUCTAL GRAY; SPINAL CORD;

EID: 73949159618     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.08.088     Document Type: Article

References (97)

1. Abrahams V.C., Anstee G., Richmond F.J., and Rose P.K. Neck muscle and trigeminal input to the upper cervical cord and lower medulla of the cat. Can. J. Physiol. Pharmacol. 57 (1979) 642-651
2. Ammann B., Gottschall J., and Zenker W. Afferent projections from the rat longus capitis muscle studied by transganglionic transport of HRP. Anat. Embryol. Berl. 166 (1983) 275-289
3. Apkarian A.V., and Hodge C.J. Primate spinothalamic pathways: I. A quantitative study of cells of origin of the spinothalamic pathways. J. Comp. Neurol. 288 (1989) 447-473
4. Bakker D.A., Richmond F.J.R., and Abrahams V.C. Central projections from cat suboccipital muscles-a study using transganglionic transport of horseradish-peroxidase. J. Comp. Neurol. 228 (1984) 409-421
5. Bandler R., and Shipley M.T. Columnar organization in the midbrain periaqueductal gray-modules for emotional expression. Trends Neurosci. 17 (1994) 379-389
6. Bandler R., and Keay K.A. Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. Prog. Brain Res. 107 (1996) 285-300
7. Bandler R., Carrive P., and Depaulis A. Introduction: emerging principles of organization of the midbrain periaqueductal gray matter. In: Depaulis A., and Bandler R. (Eds). The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization (1991), Plenum Press, New York 1-8
8. Bandler R., Keay K.A., Floyd N., and Price J. Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Res. Bull. 53 (2000) 95-104
9. Behbehani M.M., and Fields H.L. Evidence that an excitatory connection between the periaqueductal gray and nucleus raphe magnus mediates stimulation produced analgesia. Brain Res. 170 (1979) 85-95
10. Berman A.L. The Brainstem of the Cat, A Cytoarchitectonic Atlas with Stereotaxis Coordinates (1968), University of Wisconsin Press, Madison
11. Bjorkeland M., and Boivie J. Anatomy of the midbrain projections from the lateral cervical nucleus in the cat. In: Rowe M., and Willis W.D. (Eds). Development, Organization, and Processing in Somatosensory Pathways (1985), Alan, R. Liss, New York 203-214
12. Blomqvist A., Flink R., Bowsher D., Griph S., and Westman J. Tectal and thalamic projections of dorsal column and lateral cervical nuclei: a quantitative study in the cat. Brain Res. 141 (1978) 335-341
13. Burstein R., Cliffer K.D., and Giesler G.J. Cells of origin of the spinohypothalamic tract in the rat. J. Comp. Neurol. 291 (1990) 329-344
14. Burstein R., Dado R.J., and Giesler G.J. The cells of origin of the spinothalamic tract of the rat-a quantitative reexamination. Brain Res. 511 (1990) 329-337
15. Burton H., and Loewy A.D. Descending projections from marginal cell layer and other regions of monkey spinal-cord. Brain Res. 116 (1976) 485-491
16. Carstens E., and Trevino D.L. Anatomical and physiological properties of ipsilaterally projecting spinothalamic neurons in the second cervical segment of the cat's spinal cord. J. Comp. Neurol. 182 (1978) 167-184
17. Carstens E., and Trevino D.L. Laminar origins of spinothalamic projections in the cat as determined by the retrograde transport of horseradish peroxidase. J. Comp. Neurol. 182 (1978) 151-166
18. Chandler M.J., Zhang J., and Foreman R.D. Vagal, sympathetic and somatic sensory inputs to upper cervical (C1-C3) spinothalamic tract neurons in monkeys. J. Neurophysiol. 76 (1996) 2555-2567
19. Chandler M.J., Zhang J.H., and Foreman R.D. Phrenic nerve inputs to upper cervical (C1-C3) spinothalamic tract neurons in monkeys. Brain Res. 798 (1998) 93-100
20. Chandler M.J., Qin C., Yuan Y., and Foreman R.D. Convergence of trigeminal input with visceral and phrenic inputs on primate C1-C2 spinothalamic tract neurons. Brain Res. 829 (1999) 204-208
21. Chandler M.J., Zhang J.H., Qin C., and Foreman R.D. Spinal inhibitory effects of cardiopulmonary afferent inputs in monkeys: neuronal processing in high cervical segments. J. Neurophysiol. 87 (2002) 1290-1302
22. Clement C.I., Keay K.A., Podzebenko K., Gordon B.D., and Bandler R. Spinal sources of noxious visceral and noxious deep somatic afferent drive onto the ventrolateral periaqueductal gray of the rat. J. Comp. Neurol. 425 (2000) 323-344
23. Comans P.E., and Snow P.J. Rostrocaudal and laminar distribution of spinothalamic neurons in the high cervical spinal cord of the cat. Brain Res. 223 (1981) 123-127
24. Craig A.D. Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J. Comp. Neurol. 361 (1995) 225-248
25. Craig A.D. Retrograde analyses of spinothalamic projections in the macaque monkey: input to the ventral lateral nucleus. J. Comp. Neurol. 508 (2008) 315-328
26. Dutton R.C., Carstens M.I., Antognini J.F., and Carstens E. Long ascending propriospinal projections from lumbosacral to upper cervical spinal cord in the rat. Brain Res. 1119 (2006) 76-85
27. Flink R., and Svensson B.A. Fluorescent double-labelling study of ascending and descending neurones in the feline lateral cervical nucleus. Exp. Brain Res. 62 (1986) 479-485
28. Flink R., Wiberg M., and Blomqvist A. The termination in the mesencephalon of fibres from the lateral cervical nucleus. An anatomical study in the cat. Brain Res. 259 (1983) 11-20
29. Flink R., Wiberg M., and Blomqvist A. The termination in the mesencephalon of fibres from the lateral cervical nucleus. An anatomical study in the cat. Brain Res. 259 (1983) 11-20
30. Gholami S., Lambertz D., Hoheisel U., and Mense S. Effects on c-Fos expression in the PAG and thalamus by selective input via tetrodotoxin-resistant afferent fibres from muscle and skin. Neurosci. Res. 56 (2006) 270-278
31. Giesler G.J., Menetrey D., and Basbaum A.I. Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat. J. Comp. Neurol. 184 (1979) 107-125
32. Giesler G.J.J., Bjorkeland M., Xu Q., and Grant G. Organization of the spinocervicothalamic pathway in the rat. J. Comp. Neurol. 268 (1988) 223-233
33. Granum S.L. The spinothalamic system of the rat. I. Locations of cells of origin. J. Comp. Neurol. 247 (1986) 159-180
34. Hodge C.J., and Apkarian A.V. The spinothalamic tract. Crit. Rev. Neurobiol. 5 (1990) 363-397
35. Isu N., Thomson D.B., and Wilson V.J. Vestibulospinal effects on neurons in different regions of the gray matter of the cat upper cervical cord. J. Neurophysiol. 76 (1996) 2439-2446
36. Katter J.T., Burstein R., and Giesler G.J. The cells of origin of the spinohypothalamic tract in cats. J. Comp. Neurol. 303 (1991) 101-112
37. Kavia R.B., DasGupta R., and Fowler C.J. Functional imaging and the central control of the bladder. J. Comp. Neurol. 493 (2005) 27-32
38. Keay K.A., and Bandler R. Anatomical evidence for segregated input from the upper cervical spinal cord to functionally distinct regions of the periaqueductal gray region of the cat. Neurosci. Lett. 139 (1992) 143-148
39. Keay K.A., and Bandler R. Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci. Biobehav. Rev. 25 (2001) 669-678
40. Keay K.A., Clement C.I., Owler B., Depaulis A., and Bandler R. Convergence of deep somatic and visceral nociceptive information onto a discrete ventrolateral midbrain periaqueductal gray region. Neuroscience 61 (1994) 727-732
41. Keay K.A., Feil K., Gordon B.D., Herbert H., and Bandler R. Spinal afferents to functionally distinct periaqueductal gray columns in the rat: an anterograde and retrograde tracing study. J. Comp. Neurol. 385 (1997) 207-229
42. Keay K.A., Li Q.F., and Bandler R. Muscle pain activates a direct projection from ventrolateral periaqueductal gray to rostral ventrolateral medulla in rats. Neurosci. Lett. 290 (2000) 157-160
43. Keay K.A., Clement C.I., Depaulis A., and Bandler R. Different representations of inescapable noxious stimuli in the periaqueductal gray and upper cervical spinal cord of freely moving rats. Neurosci. Lett. 313 (2001) 17-20
44. Kevetter G.A., and Willis W.D. Collaterals of spinothalamic cells in the rat. J. Comp. Neurol. 215 (1983) 453-464
45. Klop E.M., Mouton L.J., and Holstege G. Nucleus retroambiguus projections to the periaqueductal gray in the cat. J. Comp. Neurol. 445 (2002) 47-58
46. Klop E.M., Mouton L.J., Ehling T., and Holstege G. Two parts of the nucleus prepositus hypoglossi project to two different subdivisions of the dorsolateral periaqueductal gray in cat. J. Comp. Neurol. 492 (2005) 303-322
47. Klop E.M., Mouton L.J., and Holstege G. Segmental and laminar organization of the spinothalamic neurons in cat: evidence for at least five separate clusters. J. Comp. Neurol. 493 (2005) 580-595
48. Klop E.M., Mouton L.J., Hulsebosch R., Boers J., and Holstege G. In cat four times as many lamina I neurons project to the parabrachial nuclei and twice as many to the periaqueductal gray as to the thalamus. Neuroscience 134 (2005) 189-197
49. Klop E.M., Mouton L.J., Kuipers R., and Holstege G. Neurons in the lateral sacral cord of the cat project to periaqueductal grey, but not to thalamus. Eur. J. Neurosci. 21 (2005) 2159-2166
50. Klop E.M., Mouton L.J., and Holstege G. Periparabigeminal and adjoining mesencephalic tegmental field projections to the dorsolateral periaqueductal grey in cat-a possible role for oculomotor input in the defensive system. Eur. J. Neurosci. 23 (2006) 2145-2157
51. Kuipers R., and Klop E.M. Neurons in the guinea pig (Cavia porcellus) lateral lumbosacral spinal cord project to the central part of the lateral periaqueductal gray matter. Brain Res. 1101 (2006) 43-50
52. Li J.L., and Mizuno N. Parabrachial nucleus neurons providing axons to both the thalamus and the spinal cord in the rat. Brain Res. 745 (1997) 321-327
53. Lonstein J.S., and Stern J.M. Role of the midbrain periaqueductal gray in maternal nurturance and aggression: c-fos and electrolytic lesion studies in lactating rats. J. Neurosci. 17 (1997) 3364-3378
54. Matsushita M., Ikeda M., and Hosoya Y. Location of spinal neurons with long descending axons (long descending propriospinal tract neurons) in the cat-study with the horseradish-peroxidase technique1. J. Comp. Neurol. 184 (1979) 63-79
55. Menetrey D., Chaouch A., Binder D., and Besson J.M. The origin of the spinomesencephalic tract in the rat: an anatomical study using the retrograde transport of horseradish peroxidase. J. Comp. Neurol. 206 (1982) 193-207
56. Mesulam M.M. Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26 (1978) 106-117
57. Miller K.E., Douglas V.D., Richards A.B., Chandler M.J., and Foreman R.D. Propriospinal neurons in the C1-C2 spinal segments project to the L5-S1 segments of the rat spinal cord7. Brain Res. Bull. 47 (1998) 43-47
58. Molenaar I., and Kuypers H.G.J.M. Identification of cells of origin of long fiber connections in the cat's spinal cord by means of the retrograde axonal horseradish peroxidase technique. Neurosci. Lett. 1 (1975) 193-197
59. Molenaar I., and Kuypers H.G.J.M. Cells of origin of propriospinal, ascending supraspinal and medullospinal fibers. A HRP study in cat and Rhesus monkey. Brain Res. 152 (1978) 429-450
60. Mouton L.J., and Holstege G. The periaqueductal gray in the cat projects to lamina VIII and the medial part of lamina VII throughout the length of the spinal cord. Exp. Brain Res. 101 (1994) 253-264
61. Mouton L.J., and Holstege G. Segmental and laminar organization of the spinal neurons projecting to the periaqueductal gray (PAG) in the cat suggests the existence of at least five separate clusters of spino-PAG neurons. J. Comp. Neurol. 428 (2000) 389-410
62. Morgan M.M., and Carrive P. Activation of the ventrolateral periaqueductal gray reduces locomotion but not mean arterial pressure in awake, freely moving rats. Neuroscience 102 (2001) 905-910
63. Mouton L.J., VanderHorst V.G.J.M., and Holstege G. Large segmental differences in the spinal projections to the periaqueductal gray in the cat. Neurosci. Lett. 238 (1997) 1-4
64. Mouton L.J., Klop E., and Holstege G. Lamina I-periaqueductal gray (PAG) projections represent only a limited part of the total spinal and caudal medullary input to the PAG in the cat. Brain Res. Bull. 54 (2001) 167-174
65. Mouton L.J., Klop E.M., Broman J., Zhang M., and Holstege G. Lateral cervical nucleus projections to periaqueductal gray matter in cat. J. Comp. Neurol. 471 (2004) 434-445
66. Mouton L.J., Klop E.M., and Holstege G. C1-C3 spinal cord projections to periaqueductal gray and thalamus: a quantitative retrograde tracing study in cat. Brain Res. 1043 (2005) 87-94
67. Mysicka A., and Zenker W. Central projections of muscle afferents from the sternomastoid nerve in the rat. Brain Res. 211 (1981) 257-265
68. Nagata T., and Kruger L. Tactile neurons of the superior colliculus of the cat-input and physiological-properties. Brain Res. 174 (1979) 19-37
69. Nyberg G., and Blomqvist A. The central projection of muscle afferent fibers to the lower medulla and upper spinal cord: an anatomical study in the cat with the transganglionic transport method. J. Comp. Neurol. 230 (1984) 99-109
70. Panfil C., Makowska A., and Ellrich J. Brainstem and cervical spinal cord Fos immunoreactivity evoked by nerve growth factor injection into neck muscles in mice. Cephalal 26 (2006) 128-135
71. Pechura C.M., and Liu R.P. Spinal neurons which project to the periaqueductal gray and the medullary reticular formation via axon collaterals: a double-label fluorescence study in the rat. Brain Res. 374 (1986) 357-361
72. Pfaller K., and Arvidsson J. Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J-Comp-Neurol 268 (1988) 91-108
73. Potas J.R., Keay K.A., Henderson L.A., and Bandler R. Somatic and visceral afferents to the "vasodepressor region" of the caudal midline medulla in the rat. Eur. J. Neurosci. 17 (2003) 1135-1149
74. Price J.L. Free will versus survival: brain systems that underlie intrinsic constraints on behavior. J. Comp. Neurol. 493 (2005) 132-139
75. Qin C., Chandler M.J., Miller K.E., and Foreman R.D. Responses and afferent pathways of superficial and deeper C-1-C-2 spinal cells to intrapericardial algogenic chemicals in rats. J. Neurophysiol. 85 (2001) 1522-1532
76. Qin C., Chandler M.J., Miller K.E., and Foreman R.D. Responses and afferent pathways of C-1-C-2 spinal neurons to gastric distension in rats. Auton. Neurosci. Basic Clin. 104 (2003) 128-136
77. Qin C., Chandler M.J., Jou C.J., and Foreman R.D. Responses and afferent pathways of C-1-C-2 spinal neurons to cervical and thoracic esophageal stimulation in rats. J. Neurophysiol. 91 (2004) 2227-2235
78. Razook J.C., Chandler M.J., and Foreman R.D. Phrenic afferent input excites C1-C2 spinal neurons in rats. Pain 63 (1995) 117-125
79. Rose P.K., and Keirstead S.A. Segmental projection from muscle spindles: a perspective from the upper cervical cord. Can. J. Physiol. Pharmacol. 64 (1986) 505-508
80. Smith M.V., and Hodge C.J. Response properties of upper cervical spinothalamic neurons in cats-a possible explanation for the unusual sensory symptoms associated with upper cervical lesions in humans. Spine 17 (1992) S375-S382
81. Smith M.V., Apkarian A.V., and Hodge C.J. Response properties of contralaterally projecting spinothalamic neurons in the second cervical segments of cat. Soc. Neurosci. Abstr. 14 (1988) 120
82. Smith M.V., Apkarian A.V., and Hodge Jr. C.J. Somatosensory response properties of contralaterally projecting spinothalamic and nonspinothalamic neurons in the second cervical segment of the cat. J. Neurophysiol. 66 (1991) 83-102
83. Trevino D.L., and Carstens E. Confirmation of the location of spinothalamic neurons in the cat and monkey by the retrograde transport of horseradish peroxidase. Brain Res. 98 (1975) 177-182
84. VanderHorst V.G.J.M., and Holstege G. A concept for the final common pathway of vocalization and lordosis behavior in the cat. Prog. Brain Res. 107 (1996) 327-342
85. VanderHorst V.G.J.M., Mouton L.J., Blok B.F.M., and Holstege G. Distinct cell groups in the lumbosacral cord of the cat project to different areas in the periaqueductal gray. J. Comp. Neurol. 376 (1996) 361-385
86. Verburgh C.A., and Kuypers H.G. Branching neurons in the cervical spinal cord: a retrograde fluorescent double-labeling study in the rat. Exp. Brain Res. 68 (1987) 565-578
87. Vianna D.M.L., and Brandao M.L. Anatomical connections of the periaqueductal gray: specific neural substrates for different kinds of fear. Braz. J. Med. Biol. Res. 36 (2003) 557-566
88. Walker P., and Carrive P. Role of ventrolateral periaqueductal gray neurons in the behavioral and cardiovascular responses to contextual conditioned fear and poststress recovery. Neuroscience 116 (2003) 897-912
89. Wiberg M., and Blomqvist A. The spinomesencephalic tract in the cat: its cells of origin and termination pattern as demonstrated by the intraaxonal transport method. Brain Res. 291 (1984) 1-18
90. Wiberg M., Westman J., and Blomqvist A. Somatosensory projection to the mesencephalon: an anatomical study in the monkey. J. Comp. Neurol. 264 (1987) 92-117
91. Yezierski R.P. Spinomesencephalic tract: projections from the lumbosacral spinal cord of the rat, cat, and monkey. J. Comp. Neurol. 267 (1988) 131-146
92. Yezierski R.P. Somatosensory input to the periaqueductal gray: a spinal relay to a descending control center. In: Depaulis A., and Bandler R. (Eds). The Midbrain Periaqueductal Gray Matter. In The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization (1991), Plenum Press, New York 365-386
93. Yezierski R.P., and Broton J.G. Functional properties of spinomesencephalic tract (SMT) cells in the upper cervical spinal cord of the cat. Pain 45 (1991) 187-196
94. Yezierski R.P., and Mendez C.M. Spinal distribution and collateral projections of rat spinomesencephalic tract cells. Neuroscience 44 (1991) 113-130
95. Yezierski R.P., Culberson J.L., and Brown P.B. Cells of origin of propriospinal connections to cat lumbosacral gray as determined with horseradish-peroxidase1. Exp. Neurol. 69 (1980) 493-512
96. Zhang D.X., Carlton S.M., Sorkin L.S., and Willis W.D. Collaterals of primate spinothalamic tract neurons to the periaqueductal gray. J. Comp. Neurol. 296 (1990) 277-290
97. Zhang J., Chandler M.J., and Foreman R.D. Cardiopulmonary sympathetic and vagal afferents excite C1-C2 propriospinal cells in rats. Brain Res. 969 (2003) 53-58