Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys

Journal of Comparative Neurology

Volumn 401, Issue 4, 1998, Pages 455-479

  An, X ^a   Bandler, R ^b,c   Ongur D ^a   Price, J L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ROYAL NORTH SHORE HOSPITAL   (Australia)

Author keywords

Amygdala; Autonomic nervous system; Emotion; Macaca fascicularis; Prefrontal cortex; Visceral control

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUTONOMIC INNERVATION; BRAIN MAPPING; EMOTION; FEMALE; MACACA; MALE; MESENCEPHALON; NERVE CELL NETWORK; NERVE PROJECTION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PREFRONTAL CORTEX; PRIORITY JOURNAL;

AMIDINES; AMYGDALA; ANIMALS; AUTONOMIC NERVOUS SYSTEM; BIOTIN; CHOLERA TOXIN; DEXTRANS; EMOTIONS; FEMALE; FLUORESCENT DYES; GYRUS CINGULI; LEUCINE; MACACA FASCICULARIS; MACACA NEMESTRINA; MALE; NEURAL PATHWAYS; NEURONS, AFFERENT; PERIAQUEDUCTAL GRAY; PREFRONTAL CORTEX; RHODAMINES; TEMPORAL LOBE; TRITIUM;

EID: 0032583097     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19981130)401:4<455::AID-CNE3>3.0.CO;2-6     Document Type: Article

References (111)

1. Abols, I.A. and A.I. Basbaum (1981) Afferent connections of the rostral medulla of the cat: a neural substrate for midbrain-medullary interactions in the modulation of pain. J. Comp. Neurol. 207:285-297
2. Bandler, R. (1988) Brain mechanisms of aggression as revealed by electrical and chemical stimulation: suggestion of a central role for the midbrain periaqueductal grey region. In A. Epstein and A. Morrison (eds): Progress in Psychobiology and Physiological Psychology, Vol. 13. New York: Academic Press, pp. 67-153.
3. Bandler, R. and A. Depaulis (1991) Midbrain periaqueductal gray control of defensive behavior in the cat and the rat. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization. New York: Plenum, pp. 175-198.
4. Bandler, R. and K.A. Keay (1996) Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. Prog. Brain Res. 107.-285-313.
5. Bandler, R. and M.T. Shipley (1994) Columnar organization in the midbrain periaqueductal gray: Modules for emotional expression? TINS 17:379-389.
6. Bandler, R., T. McCulloch, and B. Dreher (1985) Afferents to a midbrain periaqueductal grey region involved in the 'defence reaction' in the cat as revealed by horseradish peroxidase. I. The telencephalon. Brain Res. 330:109-119.
7. Bandler, R., P. Carrive, and S.P. Zhang (1991) Integration of somatic and autonomic reactions within the midbrain periaqueductal gray: Viscerotopic, somatotopic and functional organization. Prog. Brain Res. 87:67-154.
8. Bechara, A., H. Damasio, D. Tranel, and A.R. Damasio (1997) Deciding advantageously before knowing the advantageous strategy. Science 275:1293-1295.
9. Beckstead, R.M. (1979) An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat. J. Comp. Neurol. 184: 43-62.
10. Beitz, A.J. (1982) The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7:133-159.
11. Beitz, A.J. (1995) Periaqueductal gray In G. Paxinos (ed): The Rat Nervous System. San Diego: Academic Press, pp. 173-182.
12. Blomqvist, A. and A.D. Craig (1991) Organization of spinal and trigeminal inputs to the PAG. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter. New York: Plenum Press, pp. 345-364.
13. Bragin, E.O., Z.V. Yeliseeva, G.F. Vasilenko, E.E. Meizerov, B.T. Chuvin, and R.A. Durinyan (1984) Cortical projections to the periaqueductal grey in the cat: A retrograde horseradish peroxidase study. Neurosci. Lett. 51:271-215.
14. Burns, S.M. and J.M. Wyss (1985) The involvement of the anterior cingulate cortex in blood pressure control. Brain Res. 340:71-77.
15. Cameron, A.A., I.A. Khan, K.N. Westlund, and W.I. Willis (1995) The efferent projections of the periaqueductal gray in the rat: A Phaseolus vulgaris-leucoagglutinin study. II. Descending projections. J. Comp. Neurol. 357:585-601.
16. Carmichael, S.T. and J.L. Price (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J. Comp. Neurol. 346:366-402.
17. Carmichael, S.T. and J.L. Price (1995a) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 363:615-641.
18. Carmichael, S.T. and J.L. Price (1995b) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J. Comp. Neurol. 363:642-664.
19. Carmichael, S.T. and J.L. Price (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J. Comp. Neurol. 371:179-207.
20. Carmichael, S.T., M.-C. Clugnet, and J.L. Price (1994) Central olfactory connections in the macaque monkey. J. Comp. Neurol. 346:366-402.
21. Carrive, P. (1991) Functional organization of PAG neurons controlling regional vascular beds. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization. New York: Plenum, pp. 67-100.
22. Carrive, P. and R. Bandler (1991) Viscerotopic organization of neurons subserving hypotensive reactions within the midbrain periaqueductal gray: A corelative anatomical and functional study. Brain Res. 541:206-215.
23. Carrive, P and G. Paxinos (1994) The supraoculomotor cap: A region revealed by NADPH diaphorase histochemistry. NeuroReport 5:2257-2260.
24. Chen, S. and G. Aston-Jones (1996) Extensive projections from the midbrain periaqueductal to the cudal ventrolateral medulla: A retrograde and anterograde tracing study in the rat. Neuroscience 71:443-459.
25. Coffield, J.A., K.K. Bowen, and V. Miletic (1992) Retrograde tracing of projections between the nucleus submedius, the ventrolateral orbital cortex, and the midbrain in the rat. J. Comp. Neurol. 321:488-499.
26. Conti, F., P. Barbaresi, and M. Fabri (1988) Cytochrome oxidase histochemistry reveals regional subdivisions in the rat periaqueductal gray matter. Neuroscience 24:629-33
27. Cowan, W.M., D.I. Gottieb, A.E. Hendersen, J.L. Price, and T.A. Woolsey (1972) The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res. 37:21-55.
28. Craig, A.D. (1995) Distribution of brainstem projections from spinal lamina I neurons in the cat and monkey. J. Comp. Neurol. 361:225-248.
29. Dampney, R.A.L. (1994) Functional organization of pathways regulating the cardiovascular system. Physiol. Rev. 74:323-364.
30. Davis, P.J., S.P. Zhang, and R. Bandler (1996) Midbrain and medullary regulation of respiration and vocalization. Prog. Brain Res. 107:316-325.
31. Depaulis, A., K.A. Keay, and R. Bandler (1992) Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp. Brain Res. 90:307-318.
32. Depaulis, A., K.A. Keay, and R. Bandler (1994) Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat. Exp. Brain Res. 99:75-83.
33. Domesick, V.B (1969) Projections from the cingulate cortex in the rat. Brain Res. 12:296-320.
34. Drevets, W.C. and M.E. Raichle (1994) PET imaging studies of human emotional dosorders. In M.S. Gazzaniga (ed): The Cognitive Neurosciences. Cambridge, MA: MIT Press, pp. 1153-1164.
35. Drevets, W.C., T.O. Videen, S.H. Preskorn, J.L. Price, S.T. Carmichael, and M.E. Raichle (1992) A functional anatomical study of unipolar depression. J. Neurosci. 12:3628-3641.
36. Drevets, W.C., J.L. Price, J.R. Simpson, R. Todd, T. Reich, M. Vannier, and M. Raichle (1997) Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824-827.
37. Fanselow, M. (1991) The midbrain periaqueductal gray as a coordinator of acton in response to fear and anxiety. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter. New York: Plenum Press, pp. 151-173.
38. Fanselow, M. (1994) Neural organization of the defensive behavior system responsible for fear. Psychonom. Bull. Rev. 1:429-438.
39. Fernandez De Molina, A. and R. W. Hunsperger (1962) Organization of the subcortical system governing defence and flight reactions in the cat. J. Physiol. 160:200-213.
40. Fields, H.L. and A.I. Basbaum (1978) Brainstem control of spinal paintransmission neurons. Ann Rev. Physiol. 40:217-248.
41. Freedman, L.J., J.-F. Pare, T.R. Insel, and Y. Smith (1997) Subcortical projections of macaque infralimbic cortex (Area 25). Soc. Neurosci. Abstr. 23:901.
42. Goldman-Rakic, P.S. and L.J. Porrino (1985) The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J. Comp. Neurol. 242:535-560.
43. Graeff, F.G. (1990) Brain defense systems and anxiety. In G.d. Burrows, M. Roth, and R. Noyes, Jr. (eds): Handbook of Anxiety, Vol. 3. Amsterdam: Elsevier, pp. 307-354.
44. Gundlach, A.L. (1991) Regional subdivisions in the midbrain periaqueductal gray of the cat revealed by in vitro receptor autoradiography. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Grsay Matter. New York: Plenum Press, pp. 449-464.
45. Hardy, S.G. (1986) Projections to the midbrain from the medial versus lateral prefrontal cortices of the rat. Neurosci. Lett. 63:159-164.
46. Henderson, L.A., K.A. Keay, and R. Bandler (1998) The ventrolateral periaqueductal gray projects to caudal brainstem depressor regions: A functional-anatomical and physiological study. Neuroscience 82:201-221.
47. Herbert, H. and C.B. Saper (1992) Organization of medullary adrenergic and noradrenergic projections to the periaqueductal gray matter in the rat. J. Comp. Neurol. 315:34-52.
48. Herrero, M.T., R. Insausti, and L.M. Gonzalo (1991) Cortically projecting cells in the periaqueductal gray matter of the rat. A retrograde fluorescent tracer study. Brain Res. 543:201-212.
49. Hilton, S.M. (1982) The defence-arousal system and its relevance for circulatory and respiratory control. J. Exp. Biol. 100:159-174.
50. Hilton, S.M. and A.W. Zbrozyna (1963) Amygdaloid region for defence reactions and its efferent pathway to the brain stem. J. Physiol. 165:160-173
51. Holstege, G. (1989) An anatomical study on the final common pathway for vocalization in the cat. J. Comp. Neurol. 284:242-252.
52. Holstege, G. (1991) Descending pathways from the periaqueductal gray and adjacent areas. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization. New York: Plenum, pp. 239-265.
53. Hurley, K.M., H. Herbert, M.M. Moga, and C.B. Saper (1991) Efferent projections of the infralimbic cortex of the rat. J. Comp. Neurol. 308:249-276.
54. Illing, R.-B. and A.M. Graybiel (1986) Complementary and non-matching afferent compartments in the cat's superior colliculus: Innervation of the acetylcholinesterase-poor domain of the intermediate gray layer. Neuroscience 18:373-394.
55. Illinsky, I.A., M.L. Jouandet, and P.S. Goldman-Rakic (1985) Organization of the nigrothalamocortical system in the rhesus monkey. J. Comp. Neurol. 236:315-330.
56. Jürgens, U. (1991) Neurochemical study of PAG control of vocal behavior. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter. New York: Plenum Press, pp. 11-21.
57. Jürgens, U. and P. Müller-Preuss (1977) Convergent projections of different limbic vocalization areas in the squirrel monkey. Exp Brain Res. 29:75-83.
58. Jürgens, U and R. Pratt (1979) The cingular vocalization pathway in the squirrel monkey. Exp. Brain Res. 34:499-510.
59. Kaada, B. (1967) Brain mechanisms related to aggressive behavior. In C.D. Clemente and D.B. Lindsley (eds): Aggression and Defense: Neural Mechanisms and Social Patterns. Los Angeles: Univ. Calif. Press, pp. 95-134.
60. Keay, K.A., K. Feil, B. Gordon, H. Herbert, and R. Bandler (1997) Spinal afferents to functionally distinct PAG columns in the rat: An anterograde and retrograde tracing study. J. Comp. Neurol. 385:207-229.
61. Lane, R.D., E.M. Reiman, G.L.Ahern, G.E Schwartz, and R.J. Davidson (1997) Neuroanatomical correlates of happiness, sadness, and disgust. Am. J. Psychiat. 154:926-933.
62. Larson, C.R. and M.K. Kistler (1986) The relationship of periaqueductal gray neurons to volcalization and laryngeal EMG in the behaving monkey. Exp. Brain Res. 63:596-605.
63. Leichnetz, G.R. R.F. Spencer, S.G. Hardy, and J. Astruc (1981) The prefrontal corticotectal projection in the monkey; an anterograde and retrograde horseradish peroxidase study. Neuroscience 6:1023-1041.
64. Liu, H., S.Chandler, A.J.Beitz, M.T. Shipley, and M.M. Behbehani (1994) Characterization of the effect of cholecystokinin (CCK) on neurons in the periaquedutal gray of the rat: Immunohistochemical and in vivo and in vitro electrophysiological studies. Brain Res. 642:83-94.
65. Lovick, T.A. (1993) Integrated activity of cardiovascular and pain regulatory systems: Role in adaptive behavioral responses. Prog. Neurobiol. 40:631-644.
66. Lovick, T.A. (1996) Midbrain and medullary regulation of defensive cardiovascular functions. Prog. Brain Res. 107:301-313.
67. Marchand, J.E. and N. Hagino (1983) Afferents to the periaqueductal gray in the rat. A horseradish peroxidase study. Neuroscience 9:95-106.
68. Mason, P and C.G. Leung (1996) Physiological functions of pontomedullry raphe and medial reticular neurons. Prog. Brain Res. 107:269-282.
69. Meller, S.T. and B.J. Dennis (1986) Afferent projections to the periaqueductal gray in the rabbit. Neuroscience 19:927-964.
70. Mitchell, I.J., P. Dean, and P. Redgrave (1988) The projection from superior colliculus to cuneiform area in the rat. II. Defence-like responses to stimulation with glutamate in cuneiform nucleus and surrounding structures. Exp. Brain Res. 72:626-639.
71. Neafsey, E.J. (1990) Prefrontal cortical control of the autonomie nervous system: Anatomical and physiological observations. Prog. Brain Res. 85:147-165.
72. Neafsey, E.J., K.M. Hurley-Gius, and D. Arvanitis (1986) The topographical organization of neurons in the rat medial frontal, insular and olfactory cortex projecting to the solitary nucleus, olfactory bulb, periaqueductal gray and superior colliculus. Brain Res. 377:261-270.
73. Ogawa, S., L-M. Kow, M.M. McCarthy, D.W. Pfaff, and S. Schwartz-Giblin (1991) Midbrain PAG control of female reproductive behavior: In vitro electrophysiological characterization of actions of lordosis-relevant substances. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter. New York: Plenum Press, pp 211-235.
74. Öngür, D., X. An, and J.L. Price (1998) Prefrontal cortical projections to the hypothalamus in macaque monkeys. J. Comp. Neurol. 401:480-505.
75. Paxinos, G. and C. Watson (1997) The Rat Brain in Stereotaxic Coordinates. Compact Third Edition. San Diego: Academic Press.
76. Peters, A., S.L. Palay and H.deF. Webster (1976) The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: W.B. Saunders.
77. Price, J.L. (1996) Vocalization and the orbital and medial prefrontal cortex. In P.J. Davis and N.H. Fletcher (eds): Vocal Fold Physiology: Controlling Complexity and Chaos. San Diego, London: Singular Publishing Group, Inc., pp. 171-185
78. Price, J.L. and D.G. Amaral (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J. Neurosci. 11:1242-1259.
79. Price, J.L., F.T. Russchen, and D.G. Amaral (1987) The amygdaloid complex. In Handbook of Chemical Neuroanatomy, Vol. 5: Integrated Systems of the CNS. Part I, The Limbic Region. A. Bjorklund, T. Hokfelt and L.W. Swanson (eds): Amsterdam: Elsevier Science Publishers, pp. 279-388.
80. Price, J.L., S.T. Carmichael, and W.C. Drevets (1996) Networks related to the orbital and medial prefrontal cortex: A substrate for emotional behavior? Prog. Brain Res. 107:523-536.
81. Ray, J.P. and J.L. Price (1993) The organization of the projections from the mediodorsal nucleus of the thalamus to the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 337:1-31.
82. Redgrave, P., P. Dean, and G.W. Westby (1990) Organization of the crossed tecto-reticulo-spinal projection in rat-I. Anatomical evidence for separate output channels to the periabducens area and caudal medulla. Neuroscience 37:571-584.
83. Redgrave, P., P. Dean, I.J. Mitchell, A. Odekunle, and A. Clark (1988) The projection from superior colliculus to cuneiform area in the rat. I. Anatomical studies. Exp. Brain Res. 72:611-625.
84. Reiman, E.M., R.D. Lane, G.L. Ahern, G.E. Schwartz, R.J. Davidson, K.J. Friston, L.S. Yun, and K. Chen (1997) Neuroanatomical correlates of externally and internally generated human emotion. Am. J. Psychiat. 154:918-925.
85. Rivzi, T.A., M. Ennis, M.M. Behbehani and M.T. Shipley (1991) Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity. J. Comp. Neurol. 303:121-131.
86. Rouiller, EM, V. Moret, J. Tanne, and D. Boussaoud (1996) Evidence for direct connections between the hand region of the supplementary motor area and cervical motoneurons in the macaque monkey. European J. Neurosci. 8:1055-1059.
87. Russchen, F.T., D.G. Amaral, and J.L. Price (1987) The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis. J. Comp. Neurol. 256:175-210.
88. Sakuma Y. and D.W. Pfaff (1979a) Facilitation of female reproductive behavior from mesencephalic central gray in the rat. Am. J. Physiol. 237:R278-R284.
89. Sakuma Y. and D.W. Pfaff (1979b) Mecencephalic mechanisms for integration of female reproductive behavior in the rat. Am. J. Physiol. 237:R285-R290.
90. Sesack, S.R., A.Y. Deutch, R.H. Roth, and B.S. Bunney (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290:213-242.
91. Shipley, M.T., M. Ennis, T.A. Rizvi, and M.M. Behbehani (1991) Topographical specificity of forebrain inputs to the midbrain periaqueductal gray: Evidence for discrete longitudinally organized input columns. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter. New York: Plenum, pp. 417-448.
92. Shipley, M.T., A.Z. Murphy, T.A. Rivzi, M. Ennis, M.M. Behbehani (1996) Olfaction and brainstem circuits of reproductive behavior in the rat. Prog. Brain Res. 107:355-377.
93. Smith, W.K. (1945) The functional significance of the rostral cingulate cortex as revealed by its responses to electrical excitation. J. Neurophysiol. 8:241-255.
94. Szabo, J. and W.M. Cowan (1984) A stereotaxic atlas of the brain of the cynomogolus monkey (Macaca fascicularis). J. Comp. Neurol. 222:265-300.
95. Terreberry, R.R. and E.J. Neafsey (1983) Rat medial prefrontal cortex: A visceral motor region with a direct project to the solitary nucleus. Brain Res. 278:245-249.
96. Terreberry, R.R. and E.J. Neafsey (1984) The effects of medial prefrontal cortex stimulation on the heart rate in the awake rat. Soc. Neurosci. Abstr. 10:614.
97. Törk, I. (1985) Raphe nuclei and serotonin containing systems. In G. Paxinos (ed): The Rat Nervous System, Vol. 2. Sydney: Academic Press, pp. 43-78.
98. VanBockstaele, E.J., G. Aston-Jones, V.A. Pieribone, M. Ennis, and M.T. Shipley (1991) Subregions of the periaqueductal gray topographically innervate the rostroventrolateral medulla in the rat. J Comp. Neurol. 309:305-327.
99. van der Kooy, D., L.Y. Koda, J.F. McGinty, C.R. Gerfen, and F.E. Bloom (1984) The organization of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in rat. J. Comp. Neurol. 224:1-24.
100. Van Essen, D.C. and J.H.R. Maunsell (1980) Two-dimensional maps of the cerebral cortex. J. Comp. Neurol. 191:255-281.
101. VanderHorst, V.G.J.M. and G. Holstege (1996) A concept for the final common pathway of vocalization and lordosis behavior in the cat. Prog. Brain Res. 107:327-342.
102. VanderHorst, V.G.J.M. and G. Holstege (1997) Estrogen induces axonal outgrowth in the nucleus retroambiguus-lumbosacral motoneuronal pathway in the adult female cat. J Neurosci. 17:1122-1136.
103. Velayos, J.L. and F.Reinoso-Suarez (1982) Topographic organization of the brainstem afferents to the mediodorsal thalamic nucleus. J. Comp. Neurol. 206:17-27.
104. Verberne, A.J.M. and P.G. Guyenet (1992) Midbrain central gray influence on medullary sympathoexcitatory neurons and the baroreflex in rats. Am J. Physiol. 263: R24-R33.
105. Wiberg, M. and A. Blomqvist (1984) The spinomesencephalic tract in the cat: Its cells of origin and termination pattern as demonstrated by the intraaxonal transport method. Brain Res. 297: 1-18.
106. Wiberg, M., J. Westman, and A. Blomqvist (1987) Somatosensory projection to the mesencephalon: An anatomical study in the monkey. J. Comp. Neurol. 264: 92-117.
107. Winters, W.D., R.T. Kado, and W.R. Adey (1969) A Stereotaxic Atlas for Macaca nemestrina. Berkeley, CA: University of California Press.
108. Wouterlood, F.G. and H.J. Groenewegen (1985) Neuroanatomical tracing by use of Phaseolus vulgaris leucoagglutinin (PHA-L): Electron microscopy of the PHA-L-filled neuronal somata, dendrites, axons and axon terminals. Brain Res. 326:188-191.
109. Wyss, J.M. and K. Sripanidkulchai (1984) The topography of the mesencephalic and pontine projections from the cingulate cortex of the rat. Brain Res. 293:1-15.
110. Zhang, S.P., P.J. Davis, R. Bandler, and P. Carrive (1994) Brain stem integration of vocalization: Role of the midbrain periaqueductal gray. J. Neurophysiol. 72:1337-1356.
111. Zhang, S.P., P.J. Davis, and R. Bandler (1995) Brain stem integration of vocalization: Role of the nucleus retroambigualis. J. Neurophysiol. 74:2500-2512.