Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity

Journal of Comparative Neurology - Tập 303 Số 1 - Trang 121-131 - 1991
Tilat A. Rizvi1, Matthew Ennis2,1, Michael M. Behbehani2, Michael T. Shipley1
1Division of Neurobiology, Department of Anatomy and Cell Biology, University of Cincinnati, College of Medicine, Cincinnati, Ohio 45267-0521
2Department of Biophysics and Physiology, University of Cincinnati, College of Medicine, Cincinnati, Ohio 45267-0521

Tóm tắt

AbstractPrevious reports indicate that the midbrain periaqueductal gray and the central nucleus of the amygdala are interconnected but the organization of these projections has not been characterized. We have analyzed this reciprocal circuitry using anterograde and retrograde tracing methods and image analysis. Our findings reveal that innervation of periaqueductal gray from the central nucleus of the amygdala is extensive and discretely organized along the rostrocaudal axis of periaqueductal gray. In addition, the reciprocal projection from periaqueductal gray to the central nucleus of the amygdala is more extensive and more highly organized than previously suggested.Multiple or single discrete injections of wheatgerm agglutinin‐horseradish peroxidase into several rostrocaudal levels of periaqueductal gray retrogradely labeled a substantial population of neurons, predominantly located in the medial division of the central nucleus of the amygdala. Tracer injections into the central nucleus revealed a high degree of spatial organization in the projection from this nucleus to periaqueductal gray. Two discrete longitudinally directed columns in dorsomedial and lateral/ventrolateral periaqueductal gray are heavily targeted by central amygdalar inputs throughout the rostral one‐half to two‐thirds of periaqueductal gray. Beginning at the level of dorsal raphe and continuing caudally, inputs from the central nucleus terminate more uniformly throughout the ventral half of periaqueductal gray.In addition, a substantial population of periaqueductal gray neurons were retrogradely labeled from the central nucleus of the amygdala; these were heterogeneously distributed along the rostrocaudal axis of periaqueductal gray, and included both raphe and non‐raphe neurons. Thus, the present study demonstrates that periaqueductal gray receives heavy, highly organized projections from the central nucleus of the amygdala and in turn, has reciprocal connections with the central nucleus.Previous studies have demonstrated that longitudinally organized columns of output neurons located in dorsomedial and lateral/ventrolateral periaqueductal gray project to the ventral medulla. Thus, there may be considerable overlap between the two longitudinally organized terminal input columns from the central nucleus of the amygdala and the two longitudinal columns of descending projection neurons from periaqueductal gray to the ventral medulla. The central nucleus of the amygdala has been implicated in a variety of emotional/cognitive functions ranging from fear and orienting responses, defensive and aversive reactions, associative conditioning, cardiovascular regulation, and antinociception. Many of these same functions are strongly represented in the periaqueductal gray. It is noteworthy that the present results demonstrate that lateral periaqueductal gray, a preeminent central trigger site for behavioral and autonomic components of the defense/aversion response, is heavily targeted by inputs from the central nucleus of the amygdala at all levels of periaqueductal gray. Thus, the central nucleus of the amygdala to periaqueductal gray projection may be involved in the neural integration of behavioral, antinociceptive and autonomic responses with emotional state. In addition, the present demonstration of extensive reciprocal connections between the central nucleus of the amygdala and periaqueductal gray represents a route via which functional activity represented in periaqueductal gray may gain access to a forebrain structure long implicated m the integration of the cognitive and autonomic components of emotional behavior. Thus, the periaqueductal gray to central nucleus of the amygdala projection may provide a relatively direct linkage between critical species‐preserving behavioral reactions and a forebrain structure capable of influencing multiple nodal points in the descending autonomic system.

Từ khóa


Tài liệu tham khảo

10.1016/0006-8993(80)90279-6

Andrezik J. A., 1985, The Rat Nervous System, 1

10.1016/0014-4886(68)90092-7

10.1016/0006-8993(88)91465-5

Beitz A. J., 1981, An immunohistochemical study of the rodent PAG, Anat. Rec., 199, 24A

10.1016/0306-4522(82)90157-9

10.1016/0306-4522(82)90098-7

Beitz A. J., 1982, The sites of origin of brainstem neurotensin and serotonin projections to the nucleus raphe magnus, J. Neurosci., 2, 829, 10.1523/JNEUROSCI.02-07-00829.1982

Beitz A. J., 1982, Autoradiographic localization of opiate beta‐adrenergic, cholinergic and GABA receptors in the midbrain PAG, Soc. Neurosci. Abs., 8, 265

10.1016/0006-8993(83)91292-1

10.1002/cne.902370404

10.1016/0006-8993(80)90046-3

10.1016/0006-8993(89)90449-6

10.1016/0304-3940(87)90395-8

10.1016/0006-8993(88)90378-2

10.1016/0006-8993(89)90169-8

10.1016/0006-8993(89)91176-1

10.1002/cne.902460406

10.1002/cne.902360106

10.1016/0306-4522(88)90356-9

10.1016/0006-8993(89)91284-5

10.1002/cne.902410305

10.1146/annurev.ph.40.030178.001245

10.1126/science.204998

10.1007/BF00235313

10.1037/h0044853

10.1016/0006-8993(84)90386-X

10.1016/0304-3940(87)90097-8

10.1016/0306-4522(88)90339-9

10.1016/0031-9384(80)90189-4

10.1016/0196-9781(83)90014-1

10.1007/BF00239551

Hopkins D. A., 1981, The Amygdaloid Complex. INSERM Symposium No. 20, 133

10.1016/0006-8993(87)90978-4

Jenness L., 1982, Neurotensin: Topographic distribution in rat brain by immunohistochemistry, J. Comp. Neurol., 210, 211, 10.1002/cne.902100302

Kaada B., 1972, The Neurobiology of the Amygdala, 145

10.1016/0006-8993(82)90251-7

10.1016/0031-9384(79)90304-4

10.1016/0006-8993(82)90866-6

Kerr D. I. B., 1955, Responses evoked by the brainstem by tooth stimulation, Am. J. Physiol., 183, 253, 10.1152/ajplegacy.1955.183.2.253

10.1016/0196-9781(82)90063-8

10.3181/00379727-70-17013

10.1002/cne.901780204

10.1146/annurev.ps.28.020177.000353

10.1002/cne.902060205

10.1002/cne.902620105

10.1177/26.2.24068

10.1016/0014-4886(73)90049-6

10.1002/cne.902010409

10.1523/JNEUROSCI.03-07-01437.1983

10.1523/JNEUROSCI.03-03-00603.1983

10.1016/0006-8993(82)90610-2

10.1002/cne.901860106

10.1007/BF00239016

10.1002/cne.902020304

10.1126/science.283.5400.401

Post S., 1980, Contribution to the amygdaloid projection fields in the rat: A quantitative autoradiographic study, J. Hirnforsch., 21, 199

10.1523/JNEUROSCI.01-11-01242.1981

Price J. L., 1987, Handbook of Chemical Neuroanatomy, 279

Rodgers R. J., 1977, Attenuation of morphine analgesia in rats by intraamygdaloid injection of dopamine, Brain Res., 130, 156, 10.1016/0006-8993(77)90852-6

10.1016/0006-8993(81)91155-0

10.1016/0304-3940(80)90226-8

10.1002/cne.902790307

10.1016/0361-9230(82)90040-5

10.1523/JNEUROSCI.07-07-02025.1987

10.1016/0006-8993(89)91383-8

Shipley M. T., 1989, Neuroanatomical‐Tract tracing methods 2, 331, 10.1007/978-1-4757-2055-6_13

10.1016/0006-8993(76)90086-X

10.1073/pnas.74.5.2167

10.1001/archneur.1963.00460060038004

10.1016/0006-8993(82)90532-7

Van Ootegham S., 1984, Factors affecting the sensitivity and consistency of Koelle‐Friedenwald histochemical method for localization of acetylcholinesterase, Brain Res. Bull., 12, 543, 10.1016/0361-9230(84)90170-9

10.1016/0006-8993(84)91220-4

10.1016/0304-3940(82)90249-X

10.1016/0006-8993(76)91009-X

Thông tin
Thông tin xuất bản

Journal of Comparative Neurology

Tập 303 Số 1

121-131

Thông tin tác giả