Periaqueductal gray and the region of the paralemniscal area have different functions in the control of vocalization in the neotropical bat, Phyllostomus discolor

European Journal of Neuroscience

Volumn 16, Issue 10, 2002, Pages 1974-1986

  Fenzl, T ^a   Schuller, G ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Communication; Echolocation; Kainic acid; PAG; PLA

Indexed keywords

AMINO ACID RECEPTOR STIMULATING AGENT; KAINIC ACID; COAGULATING AGENT; HALOTHANE; LIDOCAINE; ORBAT; POVIDONE IODINE;

ANIMAL; ARTICLE; AUDITORY NERVOUS SYSTEM; BAT; BREATHING; ECHOLOCATION; ELECTROSTIMULATION; MALE; PERIAQUEDUCTAL GRAY MATTER; PHYSIOLOGY; TEGMENTUM; VOCALIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; CONTROLLED STUDY; DEVICE; MICRODIALYSIS; NEUROANATOMY; NONHUMAN; PHYLLOSTOMUS DISCOLOR; PRIORITY JOURNAL;

ANIMALS; AUDITORY PATHWAYS; CHIROPTERA; ECHOLOCATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; KAINIC ACID; MALE; PERIAQUEDUCTAL GRAY; RESPIRATION; TEGMENTUM MESENCEPHALI; VOCALIZATION, ANIMAL;

EID: 0036835228     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02261.x     Document Type: Article

References (60)

1. Apfelbach, R. (1972) Electrically elicited vocalizations in the gibbon Hylobates lar (Hylobatidae), and their behavioral significance. Z. Tierpsychol., 30, 420-430.
2. Bandler, R., Carrive, P. & Dapaulis, A. (1991) Emerging principles of organization of the midbrain periaqueductal gray matter. In Depaulis, A. & Bandler, R. (eds), The Midbrain Periaqueductal Gray Matter; Functional, Anatomical and Neurochemical Organization. Plenum Press, New York, pp. 1-8.
3. Baron, G., Stephan, H. & Frahm, H.D. (1996) Comparative Neurobiology in Chiroptera. Birkhaueser Verlag, Basel, Switzerland.
4. Ben Ari, Y. & Cossart, R. (2000) Kainate, a double agent that generates seizures: Two decades of progress. Trends Neurosci., 23, 580-587.
5. Bianchi, A.L., Denavit-Saubie, M. & Champagnat, J. (1995) Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol. Rev., 75, 1-45.
6. Carrive, P. (1991) Functional organization of PAG neurons controlling regional vascular beds. In Depaulis, A. & Bandler, R. (eds), The Midbrain Periaqueductal Gray Matter; Functional, Anatomical and Neurochemical Organization. Plenum Press, New York, pp. 67-100.
7. Connelly, C.A., Dobbins, E.G. & Feldman, J.L. (1992) Pre-Botzinger complex in cats: respiratory neuronal discharge patterns. Brain Res., 590, 337-340.
8. Davis, P.J., Zhang, S.P., Winkworth, A. & Bandler, R. (1996) Neural control of vocalization: respiratory and emotional influences. J. Voice, 10, 23-38.
9. Ennis, M., Xu, S.J. & Rizvi, T.A. (1997) Discrete subregions of the rat midbrain periaqueductal gray project to nucleus ambiguus and the periambigual region. Neuroscience, 80, 829-845.
10. Esposito, A., Demeurisse, G., Alberti, B. & Fabbro, F. (1999) Complete mutism after midbrain periaqueductal gray lesion. Neuroreport, 10, 681-685.
11. Esser, K.-H. (1990) Der Einfluss von Lernprozessen auf die ontogenetische Entwicklung sozialer Laute bei der kleinen Lanzennase P. discolor. Thesis, Rheinische Friedrich-Wilhelms-Universitaet, Bonn.
12. Esser, K.H. (1994) Audio-vocal learning in a non-human mammal: the lesser spear-nosed bat Phyllostomus discolor. Neuroreport, 5, 1718-1720.
13. Esser, K.H. & Daucher, A. (1996) Hearing in the FM-bat Phyllostomus discolor: a behavioral audiogram. J. Comp. Physiol. A, 178, 779-785.
14. Esser, K.H. & Pistohl, D. (1998) The vocal repertoire of the lesser spear-nosed bat (Phyllostomus discolor). Zoology, 101 (Suppl. I), 84.
15. Fanselow, M.S. (1991) The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety. In Depaulis, A. & Bandler, R. (eds), The Midbrain Periaqueductal Gray Matter; Functional, Anatomical and Neurochemical Organization. Plenum Press, New York, pp. 151-173.
16. Fenton, M. (1984) Echolocation: implications for ecology and evolution of bats. Q. Rev. Biol., 59, 33-52.
17. Gallyas, F. (1979) Silver staining of myelin by means of physical development. Neurol. Res., 1, 203-209.
18. Gould, E. (1971) Studies of maternal-infant communication and development of vocalizations in the bats Myotis and Eptesicus. Commun. Behav. Biol., 5, 263-313.
19. Gould, E. (1977) Echolocation and communication. In Baker, R.J., Jones, J.K. & Carter, D.C. (eds), Biology of Bats of the New World Family Phyllostomatidae, Part II. Tech University Press, Lubbock, Texas, pp. 247-280.
20. Gould, E. (1983) Mechanisms of mammalian auditory communication. In Eisenberg, J.F. & Kleiman, D.G. (eds), Advances in the Study of Mammalian Behavior (Am. Soc. Of Mammalogists Spec. Publications, No. 7). American Society of Mammalogists, Laurence, KS, USA, pp. 265-342.
21. Huang, Z.G., Subramanian, S.H., Balnave, R.J., Turman, A.B. & Moi-Chow, C. (2000) Roles of periaqueductal gray and nucleus tractus solitarius in cardiorespiratory function in the rat brainstem. Respir. Physiol., 120, 185-195.
22. Jürgens, U. (1979) Role of the PAG in vocal expression of emotion. Brain Res., 167, 367-378.
23. Jürgens, U. (1994) The role of the periaqueductal grey in vocal behaviour. Behav. Brain Res., 62, 107-117.
24. Jürgens, U. (1998) Neuronal control of mammalian vocalization, with special reference to the squirrel monkey. Naturwissenschaften, 85, 376-388.
25. Jürgens, U. (2000) Localization of a pontine vocalization-controlling area. J. Acoust. Soc. Am., 108, 1393-1396.
26. Jürgens, U. (2002) Neural pathways underlying vocal control. Neurosci. Biobeh. Rev., 26, 235-258.
27. Jürgens, U. & Lu, C.L. (1993) The effects of periaqueductally injected transmitter antagonists on forebrain-elicited vocalization in the squirrel monkey. Eur. J. Neurosci., 5, 735-741.
28. Kalko, E.K.V. & Schnitzler, H.J. (1998) How echolocating bats approach and aquire food. In Kunz, T.H. & Racey, P.A. (eds), Bat Biology and Conservation. Smithsonian Institution Press, Washington, pp. 197-204.
29. Kanwal, J.S., Matsumura, S., Ohlemiller, K. & Suga, N. (1994) Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. J. Acoust. Soc. Am., 96, 1229-1254.
30. Kennedy, M.C. (1975) Vocalization elicited in a lizard by electrical stimulation of the midbrain. Brain Res., 91, 321-325.
31. Kirzinger, A. & Jürgens, U. (1991) Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey. Exp. Brain Res., 84, 545-560.
32. Larson, C.R. (1991) On the relation of PAG neurons to laryngeal and respiratory muscles during vocalization in the monkey. Brain Res., 552, 77-86.
33. Larson, C. & Kistler, M. (1984) Periaqueductal gray neuronal activity associated with laryngeal EMG and vocalization in the awake monkey. Neurosci. Lett., 46, 261-266.
34. Lu, C.L. & Jürgens, U. (1993) Effects of chemical stimulation in the periaqueductal gray on vocalization in the squirrel monkey. Brain Res. Bull., 32, 143-151.
35. Martin, J.R. (1976) Motivated behaviors elicited from hypothalamus, midbrain, and pons of the guinea pig (Cavia porcellus). J. Comp. Physiol. Psychol., 90, 1011-1034.
36. McGeer, P.L. & McGeer, E.G. & Hattori, T. (1978) Kainic acid as a Tool in Neurobiology. Raven Press, New York, pp. 123-139.
37. Metzner, W. (1993) An audio-vocal interface in echolocating horseshoe bats. J. Neurosci., 13, 1899-1915.
38. Metzner, W. (1996) Anatomical basis for audio-vocal integration in echolocating horseshoe bats. J. Comp. Neurol., 368, 252-269.
39. Morgan, M.M., Whitney, P.K. & Gold, M.S. (1998) Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray. Brain Res., 804, 159-166.
40. Ni, H.F., Zhang, J.X. & Harper, R.M. (1990) Respiratory-related discharge of periaqueductal gray neurons during sleep-waking states. Brain Res., 511, 319-325.
41. Ogawa, S., Kow, L.-M., McCarthy, M.M., Pfaff, D.W. & Giblin, S.S. (1991) Midbrain PAG control of female reproductive behavior: In vitro electrophysiological characterization of actions of lordosis-relevant substances. In Depaulis, A. & Bandler, R. (eds), The Midbrain Periaqueductal Gray Matter; Functional, Anatomical and Neurochemical Organization. Plenum Press, New York, pp. 211-235.
42. Olney, J.W. (1978) Neurotoxicity of excitatory amino acids. In McGeer, E.G. (ed.), Kainic Acid as a Tool in Neurobiology. Raven Press, New York, pp. 95-121.
43. Pillat, J. & Schuller, G. (1998) Audiovocal behavior of Doppler-shift compensation in the horseshoe bat survives bilateral lesion of the paralemniscal tegmental area. Exp. Brain Res., 119, 17-26.
44. Ranck, J.B. (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res., 98, 417-440.
45. Richter, D.W. & Spyer, K.M. (2001) Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends Neurosci., 24, 464-472.
46. Rother, G. & Schmidt, U. (1982) Der Einfluss visueller Information auf die Echoortung bei Phyllostomus discolor. Z. Säugetierkunde, 47, 324-334.
47. Rübsamen, R. & Betz, M. (1986) Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat, Rhinolophus rouxi. J. Comp. Physiol. A, 159, 675-687.
48. Sakamoto, T., Wada, K., Yamanaka, Y., Shiba, K. & Nakajima, Y. (1993) Effects of microinjection of a GABA antagonist into the periaqueductal gray upon electrically-induced vocalization in decerebrate cats. Neurosci. Res., 18, 235-240.
49. Schuller, G., Fischer, S. & Schweizer, H. (1997) Significance of the paralemniscal tegmental area for audio-motor control in the moustached bat, Pteronotus, p. parnellii: the afferent off efferent connections of the paralemniscal area. Eur. J. Neurosci., 9, 342-355.
50. Schuller, G., Radtke-Schuller, S. & Betz, M. (1986) A stereotaxic method for small animals using experimentally determined reference profiles. J. Neurosci. Meth., 18, 339-350.
51. Schuller, G. & Radtke-Schuller, S. (1990) Neural control of vocalization in bats: mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat. Exp. Brain Res., 79, 192-206.
52. Schwarzacher, S.W., Smith, J.C. & Richter, D.W. (1995) Pre-Botzinger complex in the cat. J. Neurophysiol., 73, 1452-1461.
53. Suga, N., Schlegel, P., Shimozawa, T. & Simmons, J. (1973) Orientation sounds evoked from echolocating bats by electrical stimulation of the brain. J. Acoust. Soc, Am., 54, 793-797.
54. Suga, N. & Yajima, Y. (1988) Auditory-vocal integration in the midbrain of the mustached bat: periaqueductal gray and reticular formation. In Newman, J.D. (ed.), The Physiological Control of Mammalian Vocalization. Plenum Press, New York, pp. 87-107.
55. Surlykke, A. & Moss, C.F. (2000) Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J. Acoust. Soc. Am., 108, 2419-2429.
56. Valentine, D.E., Sinha, S.R. & Moss, C.F. (2002) Orientating responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus. J. Comp. Physiol. A, 188, 89-108.
57. Van Bockstaele, E.J., Aston, J.G., Pieribone, V.A., Ennis M. & Shipley, M.T. (1991) Subregions of the periaqueductal gray topographically innervate the rostral ventral medulla in the rat. J. Comp. Neurol., 309, 305-327.
58. Wagner (1843) Diagnosen neuer Arten Brasilischer Handflugler. Arch. Naturgesch., 9, 365-368.
59. Yajima, Y., Hayashi, Y. & Yoshii, N. (1980) The midbrain central gray substance as a highly sensitive neural structure for the production of ultrasonic vocalization in the rat. Brain Res., 198, 445-452.
60. Zhang, S.P., Davis, P.J., Bandler, R. & Carrive, P. (1994) Brain stem integration of vocalization: role of the midbrain periaqueductal gray. J. Neurophysiol., 72, 1337-1356.