Modulation of sensory-motor integration as a general mechanism for context dependence of behavior

General and Comparative Endocrinology

Volumn 176, Issue 3, 2012, Pages 465-471

  Hoke, Kim Lisa ^a   Pitts, Natalie Lynn ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Acoustic communication; Anuran; Neuromodulation; Sensory motor gating; Social behavior network; Social decision making network

Indexed keywords

ARTICLE; AUDITORY STIMULATION; BEHAVIOR; DECISION MAKING; ENERGY EXPENDITURE; EXPERIENCE; FOREBRAIN; FROGS AND TOADS; LOCOMOTION; MESENCEPHALON; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REPRODUCTION; SENSORIMOTOR INTEGRATION; SEX; SOCIAL BEHAVIOR; STIMULUS RESPONSE;

EID: 84859903917     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.02.014     Document Type: Article

References (112)

1. Akre K.L., Ryan M.J. Female túngara frogs elicit more complex mating signals from males. Behav. Ecol. 2011, 22:846-853.
2. Allison J.D. Acoustic modulation of neural activity in the preoptic area and ventral hypothalamus of the green treefrog (Hyla cinerea). J. Comp. Physiol. A. 1992, 171:387-395.
3. Allison J.D., Wilczynski W. Thalamic and midbrain auditory projections to the preoptic area and ventral hypothalamus in the green treefrog (Hyla cinerea). Brain Behav. Evol. 1991, 38:322-331.
4. Allison J.D., Wilczynski W. Efferents from the suprachiasmatic nucleus to basal forebrain nuclei in the green treefrog (Hyla cinerea). Brain Behav. Evol. 1994, 43:129-139.
5. Attwell D., Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow. Metab. 2001, 21:1133-1145.
6. Baugh A.T., Ryan M.J. Ambient light alters temporal updating behaviour during mate choice in a neotropical frog. Can. J. Zool. 2010, 88:448-453.
7. Baugh A.T., Ryan M.J. Mate choice in response to dynamic presentation of male advertisement signals in túngara frogs. Anim. Behav. 2010, 79:145-152.
8. Bee M.A. Experience based plasticity of acoustically evoked aggression in a territorial frog. J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol. 2003, 189:485-496.
9. Bernal X.E., Akre K.L., Baugh A.T., Rand A.S., Ryan M.J. Female and male behavioral response to advertisement calls of graded complexity in túngara frogs, Physalaemus pustulosus. Behav. Ecol. Sociobiol. 2009, 63:1269-1279.
10. Bernal X.E., Rand A.S., Ryan M.J. Sex differences in response to nonconspecific advertisement calls: receiver permissiveness in male and female túngara frogs. Anim. Behav. 2007, 73:955-964.
11. Bernal X.E., Rand A.S., Ryan M.J. Sexual differences in the behavioral response of túngara frogs, Physalaemus pustulosus, to cues associated with increased predation risk. Ethology 2007, 113:755-763.
12. Bolhuis J.J., Zijlstra G.G., den Boer-Visser A.M., Van der Zee E.A. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc. Natl. Acad. Sci. USA 2000, 97:2282-2285.
13. Bonachea L.A., Ryan M.J. Predation risk increases permissiveness for heterospecific advertisement calls in túngara frogs, Physalaemus pustulosus. Anim. Behav. 2011, 82:347-352.
14. Burmeister S.S., Mangiamele L.A., Lebonville C.L. Acoustic modulation of immediate early gene expression in the auditory midbrain of female túngara frogs. Brain Res. 2008, 1190:105-114.
15. Burmeister S.S., Wilczynski W., Ryan M.J. Temporal call changes and prior experience affect graded signalling in the cricket frog. Anim. Behav. 1999, 57:611-618.
16. Buxbaum-Conradi H., Ewert J.P. Responses of single neurons in the toad's caudal ventral striatum to moving visual stimuli and test of their efferent projection by extracellular antidromic stimulation/recording techniques. Brain Behav. Evol. 1999, 54:338-354.
17. Chakraborty M., Burmeister S.S. Sexually dimorphic androgen and estrogen receptor mRNA expression in the brain of túngara frogs. Horm. Behav. 2010, 58:619-627.
18. Chakraborty M., Mangiamele L.A., Burmeister S.S. Neural activity patterns in response to interspecific and intraspecific variation in mating calls in the túngara frog. PLoS One 2010, 5:e12898.
19. Chu J., Wilczynski W. Apomorphine effects on frog locomotor behavior. Physiol. Behav. 2007, 91:71-76.
20. Clayton D.F. The genomic action potential. Neurobiol. Learn. Mem. 2000, 74:185-216.
21. Dawson B., Ryan M.J. Early experience leads to changes in the advertisement calls of male Physalaemus pustulosus. Copeia 2009, 2:221-226.
22. Deco G., Rolls E.T. Attention, short-term memory, and action selection: a unifying theory. Prog. Neurobiol. 2005, 76:236-256.
23. Diekamp B., Gerhardt H.C. Selective phonotaxis to advertisement calls in the grey treefrog Hyla versicolor: behavioral experiments and neurophysiological correlates. J. Comp. Physiol. A. 1995, 177:173-190.
24. Edwards C.J., Alder T.B., Rose G.J. Auditory midbrain neurons that count. Nat. Neurosci. 2002, 5:934-936.
25. Elliott T.M., Christensen-Dalsgaard J., Kelley D.B. Temporally selective processing of communication signals by auditory midbrain neurons. J. Neurophysiol. 2011, 105:1620-1632.
26. Endepols H., Feng A.S., Gerhardt H.C., Carl H., Schul J., Walkowiak W. Roles of the auditory midbrain and thalamus in selective phonotaxis in female gray treefrogs (Hyla versicolor). Behav. Brain Res. 2003, 145:63-77.
27. Endepols H., Roden K., Walkowiak W. Hodological characterization of the septum in anuran amphibians: II. Efferent connections. J. Comp. Neurol. 2005, 483:437-457.
28. Endepols H., Schul J., Gerhardt H.C., Walkowiak W. 6-hydroxydopamine lesions in anuran amphibians: a new model system for Parkinson's disease?. J. Neurobiol. 2004, 60:395-410.
29. Endepols H., Walkowiak W. Influence of descending forebrain projections on processing of acoustic signals and audiomotor integration in the anuran midbrain. Eur. J. Morphol. 1999, 37:182-184.
30. Endepols H., Walkowiak W. Integration of ascending and descending inputs in the auditory midbrain of anurans. J. Comp. Physiol. A. 2001, 186:1119-1133.
31. Endepols H., Walkowiak W., Luksch H. Chemoarchitecture of the anuran auditory midbrain. Brain Res. Rev. 2000, 33:179-198.
32. Ewert J.P., Buxbaum-Conradi H., Dreisvogt F., Glagow M., Merkel-Harff C., Rottgen A., Schurg-Pfeiffer E., Schwippert W.W. Neural modulation of visuomotor functions underlying prey catching behaviour in anurans: perception, attention, motor performance, learning. Comp. Biochem. Physiol. A. 2001, 128:417-461.
33. Feng A.S., Hall J.C., Gooler D.M. Neural basis of sound pattern recognition in anurans. Prog. Neurobiol. 1990, 34:313-329.
34. Feng A.S., Lin W.Y. Differential innervation patterns of three divisions of frog auditory midbrain (torus semicircularis). J. Comp. Neurol. 1991, 306:613-630.
35. Finkenstadt T., Ewert J.P. Effects of visual associative conditioning on behavior and cerebral metabolic activity in toads. Naturwissenschaften 1988, 75:95-97.
36. Freeberg T.M., Duncan S.D., Kast T.L., Enstrom D.A. Cultural influences on female mate choice: an experimental test in cowbirds, Molothrus ater. Anim. Behav. 1999, 57:421-426.
37. Fuzessery Z.M., Feng A.S. Mating call selectivity in the thalamus and midbrain of the leopard frog (Rana p. pipiens): single and multiunit analysis. J. Comp. Physiol. A. 1983, 150:333-344.
38. Gao E., Suga N. Experience dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc. Natl. Acad. Sci. USA 1998, 95:12663-12670.
39. Gao E., Suga N. Experience dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc. Natl. Acad. Sci. USA 2000, 97:8081-8086.
40. Gentner T.Q., Hulse S.H., Duffy D., Ball G.F. Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J. Neurobiol. 2001, 46:48-58.
41. Gerhardt C.H., Huber F. Acoustic Communication in Insects and Anurans 2002, The University of Chicago Press, Chicago.
42. Glagow M., Ewert J.P. Apomorphine alters prey catching patterns in the common toad: behavioral experiments and (14)C-2-deoxyglucose brain mapping studies. Brain Behav. Evol. 1999, 54:223-242.
43. Hall J.C., Feng A.S. Evidence for parallel processing in the frog's auditory thalamus. J. Comp. Neurol. 1987, 258:407-419.
44. Hebets E.A. Attention-altering signal interactions in the multimodal courtship display of the wolf spider, Schizocosa uetzi. Behav. Ecol. 2005, 16:75-82.
45. Hoke K.L., Burmeister S.S., Fernald R.D., Rand A.S., Ryan M.J., Wilczynski W. Functional mapping of the auditory midbrain during mate call reception. J. Neurosci. 2004, 24:11264-11272.
46. Hoke K.L., Ryan M.J., Wilczynski W. Functional coupling between substantia nigra and basal ganglia homologues in amphibians. Behav. Neurosci. 2007, 121:1393-1399.
47. Hoke K.L., Ryan M.J., Wilczynski W. Integration of sensory and motor processing underlying social behaviour in túngara frogs. Proc. Biol. Sci. 2007, 274:641-649.
48. Hoke K.L., Ryan M.J., Wilczynski W. Candidate neural locus for sex differences in reproductive decisions. Biol. Lett. 2008, 4:518-521.
49. Hoke K.L., Ryan M.J., Wilczynski W. Sexually dimorphic sensory gating drives behavioral differences in túngara frogs. J. Exp. Biol. 2010, 213:3463-3472.
50. K.L. Hoke, W. Wilczynski, Multifunctional neural systems and plasticity in their sensory-motor transformations, in: L. Hermer (Ed.), Reciprocal Interactions Among Early Sensory and Motor Areas and Higher Cognitive Networks, Research Signpost, Kerala, 2011.
51. E.D. Jarvis, Learned birdsong and the neurobiology of human language, in: H.P. Zeigler, P. Marler (Eds.), Behavioral Neurobiology of Birdsong, 2004, pp. 749-777.
52. Knudsen E.I. Fundamental components of attention. Annu. Rev. Neurosci. 2007, 30:57-78.
53. Laberge F., Muhlenbrock-Lenter S., Dicke U., Roth G. Thalamo-telencephalic pathways in the fire-bellied toad, Bombina orientalis. J. Comp. Neurol. 2008, 508:806-823.
54. Laberge F., Roth G. Organization of the sensory input to the telencephalon in the fire bellied toad, Bombina orientalis. J. Comp. Neurol. 2007, 502:55-74.
55. Laughlin S.B. Energy as a constraint on the coding and processing of sensory information. Curr. Opin. Neurobiol. 2001, 11:475-480.
56. Laughlin S.B., van Steveninck R.R.D., Anderson J.C. The metabolic cost of neural information. Nat. Neurosci. 1998, 1:36-41.
57. Luksch H., Walkowiak W. Morphology and axonal projection patterns of auditory neurons in the midbrain of the painted frog, Discoglossus pictus. Hear. Res. 1998, 122:1-17.
58. Lynch K.S., Wilczynski W. Reproductive hormones modify reception of species typical communication signals in a female anuran. Brain Behav. Evol. 2008, 71:143-150.
59. MacDougall-Shackleton S.A., MacDougall-Shackleton E.A., Hahn T.P. Physiological and behavioural responses of female mountain white-crowned sparrows to natal- and foreign-dialect songs. Can. J. Zool. 2001, 79:325-333.
60. Maier S., Walkowiak W., Luksch H., Endepols H. An indirect basal ganglia pathway in anuran amphibians?. J. Chem. Neuroanat. 2010, 40:21-35.
61. Mangiamele L.A., Burmeister S.S. Auditory selectivity for acoustic features that confer species recognition in the túngara frog. J. Exp. Biol. 2011, 214:2911-2918.
62. Marin O., Gonzalez A., Smeets W. Anatomical substrate of amphibian basal ganglia involvement in visuomotor behaviour. Eur. J. Neurosci. 1997, 9:2100-2109.
63. Marin O., Smeets W., Gonzalez A. Basal ganglia organization in amphibians: development of striatal and nucleus accumbens connections with emphasis on the catecholaminergic inputs. J. Comp. Neurol. 1997, 383:349-369.
64. Marin O., Smeets W., Gonzalez A. Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians. Trends Neurosci. 1998, 21:487-494.
65. Matragrano L.L., Sanford S.E., Salvante K.G., Sockman K.W., Maney D.L. Estradiol-dependent catecholaminergic innervation of auditory areas in a seasonally breeding songbird. Eur. J. Neurosci. 2011, 34:416-425.
66. Matsumoto N., Schwippert W.W., Beneke T.W., Ewert J.P. Forebrain-mediated control of visually guided prey catching in toads; investigation of striato pretectal connections with intracellular recording labeling methods. Behav. Processes 1991, 25:27-40.
67. Mei H., Chen Q. Neural modulation in inferior colliculus and central auditory plasticity. Front. Biol. 2011, 5:123-127.
68. Mello C.V., Clayton D.F. Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J. Neurosci. 1994, 14:6652-6666.
69. Mello C.V., Vicario D.S., Clayton D.F. Song presentation induces gene expression in the songbird forebrain. Proc. Natl. Acad. Sci. USA 1992, 89:6818-6822.
70. Moreno N., Gonzalez A. Hodological characterization of the medial amygdala in anuran amphibians. J. Comp. Neurol. 2003, 466:389-408.
71. Moreno N., Gonzalez A. Localization and connectivity of the lateral amygdala in anuran amphibians. J. Comp. Neurol. 2004, 479:130-148.
72. Moreno N., Gonzalez A. Forebrain projections to the hypothalamus are topographically organized in anurans: conservative traits as compared with amniotes. Eur. J. Neurosci. 2005, 21:1895-1910.
73. Mudry K.M., Capranica R.R. Evoked auditory activity within the telencephalon of the bullfrog (Rana catesbeiana). Brain Res. 1980, 182:303-311.
74. Mudry K.M., Capranica R.R. Correlation between auditory thalamic area evoked responses and species-specific call characteristics II. Hyla cinerea (Anura: Hylidae). J. Comp. Physiol. A. 1987, 161:407-416.
75. Mudry K.M., Constantine-Paton M., Capranica R.R. Auditory sensitivity of the diencephalon of leopard frog Rana p. pipiens. J. Comp. Physiol. A. 1977, 114:1-13.
76. Nagle L., Kreutzer M.L. Adult female domesticated canaries can modify their song preferences. Can. J. Zool. 1997, 75:1346-1350.
77. Narins P.M., Feng A.S., Fay R.R., Popper A.N. Hearing and Sound Communication in Amphibians 2007, Springer Science, New York.
78. Neary T.J., Wilczynski W. Auditory pathways of the hypothalamus in ranid frogs. Neurosci. Lett. 1986, 71:142-146.
79. Niven J.E., Anderson J.C., Laughlin S.B. Fly photoreceptors demonstrate energy-information trade-offs in neural coding. PLoS Biol. 2007, 5:828-840.
80. Niven J.E., Laughlin S.B. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 2008, 211:1792-1804.
81. O'Connell L.A., Ding J.H., Ryan M.J., Hofmann H.A. Neural distribution of the nuclear progesterone receptor in the túngara frog, Physalaemus pustulosus. J. Chem. Neuroanat. 2011, 41:137-147.
82. O'Connell L.A., Hofmann H.A. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol. 2011, 519:3599-3639.
83. Patton P., Grobstein P. The effects of telencephalic lesions on visually mediated prey orienting behavior in the leopard frog (Rana pipiens): I. The effects of complete removal of one telencephalic lobe, with a comparison to the effects of unilateral tectal lobe lesions. Brain Behav. Evol. 1998, 51:123-143.
84. Penna M., Lin W.Y., Feng A.S. Temporal selectivity for complex signals by single neurons in the torus semicircularis of Pleurodema thaul (Amphibia: Leptodactylidae). J. Comp. Physiol. A. 1997, 180:313-328.
85. Penna M., Lin W.Y., Feng A.S. Temporal selectivity by single neurons in the torus semicircularis of Batrachyla antartandica (Amphibia: Leptodactylidae). J. Comp. Physiol. A. 2001, 187:901-912.
86. Rand A.S., Bridarolli M.E., Dries L., Ryan M.J. Light levels influence female choice in túngara frogs: predation risk assessment?. Copeia 1997, 2:447-450.
87. Ribeiro S., Cecchi G.A., Magnasco M.O., Mello C.V. Toward a song code: evidence for a syllabic representation in the canary brain. Neuron 1998, 21:359-371.
88. Roden K., Endepols H., Walkowiak W. Hodological characterization of the septum in anuran amphibians: I. Afferent connections. J. Comp. Physiol. A. 2005, 483:415-436.
89. Rose G.J., Gooler D.M. Function of the Amphibian Central Auditory System. Hearing and Sound Communication in Amphibians 2007, 250-290. Springer Science, New York. P.M. Narins, A.S. Feng, R.R. Fay, A.N. Popper (Eds.).
90. M.J. Ryan, Anuran Communication, Smithsonian Institution, Washington, 2001.
91. Schmidt R.S. Mating call phonotaxis in female American toads: lesion of central auditory system. Brain Behav. Evol. 1988, 32:119-128.
92. Schmidt R.S. Mating call phonotaxis in female American toad: lesions of anterior preoptic nucleus. Horm. Behav. 1989, 23:1-9.
93. Schwartz J.J., Gerhardt H.C. The neuroethology of frequency preferences in the spring peeper. Anim. Behav. 1998, 56:55-69.
94. Sockman K.W., Gentner T.Q., Ball G.F. Recent experience modulates forebrain gene expression in response to mate choice cues in European starlings. Proc. Biol. Sci. 2002, 269:2479-2485.
95. Sockman K.W., Gentner T.Q., Ball G.F. Complementary neural systems for the experience dependent integration of mate choice cues in European starlings. J. Neurobiol. 2005, 62:72-81.
96. Sockman K.W., Salvante K.G. The integration of song environment by catecholaminergic systems innervating the auditory telencephalon of adult female European starlings. Dev. Neurobiol. 2008, 68:656-668.
97. Stripling R., Volman S.F., Clayton D.F. Response modulation in the zebra finch neostriatum: relationship to nuclear gene regulation. J. Neurosci. 1997, 17:3883-3893.
98. Suga N. The neural circuit for tone-specific plasticity in the auditory system elicited by conditioning. Learn. Mem. 2008, 15:198-201.
99. Taylor R.C., Klein B.A., Stein J., Ryan M.J. Multimodal signal variation in space and time: how important is matching a signal with its signaler?. J. Exp. Biol. 2011, 214:815-820.
100. Urano A., Gorbman A. Effects of pituitary hormonal treatment on responsiveness of anterior preoptic neurons in male leopard frogs, Rana p. pipiens. J. Comp. Physiol. A. 1981, 141:163-171.
101. Walkowiak W. Call production and neural basis of vocalization. Hearing and Sound Communication in Amphibians 2007, 87-112. Springer, New York. P.M. Narins, A.S. Feng, R.R. Fay, A.N. Popper (Eds.).
102. Walkowiak W., Berlinger M., Schul J., Gerhardt H.C. Significance of forebrain structures in acoustically guided behavior in anurans. Eur. J. Morphol. 1999, 37:177-181.
103. Walkowiak W., Luksch H. Sensory motor interfacing in acoustic behavior of anurans. Am. Zool. 1994, 34:685-695.
104. Wells K.D., Schwartz J.J. The behavioral ecology of anuran communication. Heaing and Sound Communication in Amphibians 2007, 44-86. Springer Science, New York. P.M. Narins, A.S. Feng, R.R. Fay, A.N. Popper (Eds.).
105. Wilczynski W. Afferents to the midbrain auditory center in the bullfrog, Rana catesbeiana. J. Comp. Neurol. 1981, 198:421-433.
106. Wilczynski W., Allison J.D. Acoustic modulation of neural activity in the hypothalamus of the leopard frog. Brain Behav. Evol. 1989, 33:317-324.
107. Wilczynski W., Endepols H. Central auditory pathways in anuran amphibians: the anatomical basis of hearing and sound communication. Hearing and Sound Communication in Amphibians 2007, 221-249. Springer, Science, New York. P.M. Narins, A.S. Feng, R.R. Fay, A.N. Popper (Eds.).
108. Wilczynski W., Lynch K.S. Female sexual arousal in amphibians. Horm. Behav. 2011, 59:630-636.
109. Wilczynski W., Lynch K.S., O'Bryant E.L. Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology. Horm. Behav. 2005, 48:440-450.
110. Wilczynski W., Northcutt R.G. Connections of the bullfrog striatum: efferent projections. J. Comp. Neurol. 1983, 214:333-343.
111. Wu G.Y., Wang S.R. Postsynaptic potentials and axonal projections of tegmental neurons responding to electrical stimulation of the toad striatum. Neurosci. Lett. 2007, 429:111-114.
112. Xiong Y., Zhang Y.H., Yan J. The neurobiology of sound-specific auditory plasticity: a core neural circuit. Neurosci. Biobehav. Rev. 2009, 33:1178-1184.