Representations of conspecific song by starling secondary forebrain auditory neurons: Toward a hierarchical framework

Journal of Neurophysiology

Volumn 103, Issue 3, 2010, Pages 1195-1208

  Meliza, C Daniel ^a   Chi, Zhiyi ^b   Margoliash, Daniel ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC NERVE FIBER; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FOREBRAIN; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RECEPTIVE FIELD; STARLING; STIMULUS; VOCALIZATION;

ACOUSTIC STIMULATION; ALGORITHMS; ANIMALS; ELECTROPHYSIOLOGY; FEMALE; LINEAR MODELS; MALE; NEURAL PATHWAYS; PROSENCEPHALON; SENSORY RECEPTOR CELLS; SPECIES SPECIFICITY; STARLINGS; VOCALIZATION, ANIMAL;

EID: 77949714049     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00464.2009     Document Type: Article

References (70)

1. Adret-Hausberger M, Jenkins PF. Complex organization of the warbling song in starlings. Behaviour 107: 138-156, 1988.
2. Aertsen AM, Johannesma PI. The spectro-temporal receptive field. A functional characteristic of auditory neurons. Biol Cybern 42: 133-143, 1981.
3. Ahrens MB, Linden JF, Sahani M. Nonlinearities and contextual influences in auditory cortical responses modeled with multilinear spectrotemporal methods. J Neurosci 28: 1929-1942, 2008.
4. Atencio CA, Sharpee TO, Schreiner CE. Cooperative nonlinearities in auditory cortical neurons. Neuron 58: 956-966, 2008.
5. Barlow HB. Pattern recognition and the responses of sensory neurons. Ann NY Acad Sci 156: 872-881, 1969.
6. Bar-Yosef O, Rotman Y, Nelken I. Responses of neurons in cat primary auditory cortex to bird chirps: effects of temporal and spectral context. J Neurosci 22: 8619-8632, 2002.
7. Bonke D, Scheich H, Langner G. Responsiveness of units in the auditory neostriatum of the guinea fowl (Numida meleagris) to species-specific calls and synthetic stimuli. J Comp Physiol [A] 132: 243-255, 1979.
8. Britten KH, Shadlen MN, Newsome WT, Movshon JA. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12: 4745-4765, 1992.
9. Capsius B, Leppelsack HJ. Influence of urethane anesthesia on neural processing in the auditory cortex analogue of a songbird. Hear Res 96: 59-70, 1999.
10. Christianson GB, Sahani M, Linden JF. The consequences of response nonlinearities for interpretation of spectrotemporal receptive fields. J Neurosci 28: 446-455, 2008.
11. Dahmen JC, King AJ. Learning to hear: plasticity of auditory cortical processing. Curr Opin Neurobiol 17: 456-464, 2007.
12. Eens M. Understanding the complex song of the European starling: an integrative approach. Adv Stud Behav 26: 355-434, 1997.
13. Eens M, Pinxten M, Verheyen RF. Temporal and sequential organization of song bouts in the European starling. Ardea 77: 75-86, 1989.
14. Eens M, Pinxten R, Verheyen RF. Male song as a cue for mate choice in the European starling. Behaviour 116: 210-238, 1991.
15. Eggermont JJ, Aertsen AMHJ, Johannesma PIM. Quantitative characterisation procedure for auditory neurons based on the spectro-temporal receptive field. Hear Res 10: 167-190, 1983.
16. Escabí MA, Nassiri R, Miller LM, Schreiner CE, Read HL. The contribution of spike threshold to acoustic feature selectivity, spike information content, and information throughput. J Neurosci 25: 9524-9534, 2005.
17. Feare CJ. The Starling. Oxford, UK: Oxford, 1984.
18. Gardner T, Cecchi G, Magnasco M, Laje R, Mindlin GB. Simple motor gestures for birdsongs. Phys Rev Lett 87: 208101, 2001.
19. Gentner TQ, Fenn KM, Margoliash D, Nusbaum HC. Recursive syntactic pattern learning by songbirds. Nature 440: 1204-1207, 2006.
20. Gentner TQ, Hulse SH. Perceptual mechanisms for individual vocal recognition in European starlings, Sturnus vulgaris. Anim Behav 56: 579-594, 1998.
21. Gentner TQ, Hulse SH. Female European starling preference and choice for variation in conspecific male song. Anim Behav 59: 443-458, 2000a.
22. Gentner TQ, Hulse SH. Perceptual classification based on the component structure of song in European starlings. J Acoust Soc Am 107: 3369-3381, 2000b.
23. Gentner TQ, Margoliash D. The neuroethology of vocal communication: perception and cognition. In: Acoustic Communications, edited by Simmons A. PANSpringer-Verlag, 2002, chapt. 7, p. 324-386.
24. Gentner TQ, Margoliash D. Neuronal populations and single cells representing learned auditory objects. Nature 424: 669-674, 2003.
25. Grace JA, Amin N, Singh NC, Theunissen FE. Selectivity for conspecific song in the zebra finch auditory forebrain. J Neurophysiol 89: 472-487, 2003.
26. Hausberger M. Social influences on song acquisition and sharing in the European starling (Sturnus vulgaris). In: Social Influences on Vocal Development, edited by Snowden C, Hausberger, M. Cambridge, MA: Cambridge, 1997, p. 128-156.
27. Hsu A, Borst A, Theunissen FE. Quantifying variability in neural responses and its application for the validation of model predictions. Network 15: 91-109, 2004.
28. Hubel DH, Wiesel TN. Receptive fields, binocular interaction, and functional architecture in cat's visual cortex. J Physiol 160: 106-156, 1962.
29. Jortner RA, Farivar SS, Laurent G. A simple connectivity scheme for sparse coding in an olfactory system. J Neurosci 27: 1659-1669, 2007.
30. Karten HJ. The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res 11: 134-153, 1968.
31. Kobatake E, Tanaka K. Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. J Neurophysiol 71: 856-867, 1994.
32. Leppelsack HJ, Vogt M. Responses of auditory neurons in the forebrain of a songbird to stimulation with species-specific sounds. J Comp Physiol [A] 107: 263-274, 1976.
33. Lewicki MS, Arthur BJ. Hierarchical organization of auditory temporal context sensitivity. J Neurosci 16: 6987-6998, 1996.
34. Liberman AM, Harris KS, Kinney JA, Lane H. The discrimination of relative onset-time of the components of certain speech and nonspeech patterns. J Exp Psychol 61: 379-388, 1961.
35. Margoliash D. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J Neurosci 3: 1039-1057, 1983.
36. Margoliash D. Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow. J Neurosci 6: 1643-1661, 1986.
37. Margoliash D, Fortune ES. Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J Neurosci 12: 4309-4326, 1992.
38. McCormick DA, Connors BW, Lighthall JW, Prince DA. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782-806, 1985.
39. Müller CM, Leppelsack HJ. Feature extraction and tonotopic organization in the avian auditory forebrain. Exp Brain Res 59: 587-599, 1985.
40. Nagel KI, Doupe AJ. Organizing principles of spectro-temporal encoding in the avian primary auditory area field L. Neuron 58: 938-955, 2008.
41. Narayan R, Best V, Ozmeral E, McClaine E, Dent M, Shinn-Cunningham B, Sen K. Cortical interference effects in the cocktail party problem. Nat Neurosci 10: 1601-1607, 2007.
42. Nelson DA, Marler P. Categorical perception of a natural stimulus continuum: birdsong. Science 244: 976-978, 1989.
43. Olshausen BA, Field DJ. Sparse coding of sensory inputs. Curr Opin Neurobiol 14: 481-487, 2004.
44. O'Neill WE, Suga N. Target range-sensitive neurons in the auditory cortex of the mustache bat. Science 203: 69-73, 1979.
45. Peña JL, Konishi M. Auditory spatial receptive fields created by multiplication. Science 292: 249-252, 2001.
46. Prather JF, Nowicki S, Anderson RC, Peters S, Mooney R. Neural correlates of categorical perception in learned vocal communication. Nat Neurosci 12: 221-228, 2009.
47. Rauschecker JP. Cortical processing of complex sounds. Curr Opin Neurobiol 8: 516-521, 1998.
48. Rauske PL, Shea SD, Margoliash D. State and neuronal class-dependent reconfiguration in the avian song system. J Neurophysiol 89: 1688-1701, 2003.
49. Ribeiro S, Cecchi GA, Magnasco MO, Mello CV. Toward a song code: evidence for a syllabic representation in the canary brain. Neuron 21: 359-371, 1998.
50. Riesenhuber M, Poggio T. Neural mechanisms of object recognition. Curr Opin Neurobiol 12: 162-168, 2002.
51. Roeder KD. Auditory system of noctuid moths. Science 154: 1515-1521, 1966.
52. Romo R, Salinas E. Flutter discrimination: neural codes, perception, memory and decision making. Nat Rev Neurosci 4: 203-218, 2003.
53. Searcy WA, Nowicki S, Peters S. Song types as fundamental units in vocal repertoires. Anim Behav 58: 37-44, 1999.
54. Sen K, Theunissen FE, Doupe AJ. Feature analysis of natural sounds in the songbird auditory forebrain. J Neurophysiol 86: 1445-1458, 2001.
55. Sharpee T, Rust NC, Bialek W. Analyzing neural responses to natural signals: maximally informative dimensions. Neural Comput 16: 223-250, 2004.
56. Sharpee TO, Miller KD, Stryker MP. On the importance of static nonlinearity in estimating spatiotemporal neural filters with natural stimuli. J Neurophysiol 99: 2496-2509, 2008.
57. Suga N. Specialization of the auditory system for reception and processing of species-specific sounds. Federation Proc 37: 2342-2354, 1978.
58. Tan AYY, Zhang LI, Merzenich MM, Schreiner CE. Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92: 630-643, 2004.
59. Theunissen FE. From synchrony to sparseness. Trends Neurosci 26: 61-64, 2003.
60. Theunissen FE, Amin N, Shaevitz SS, Woolley SMN, Fremouw T, Hauber ME. Song selectivity in the song system and in the auditory forebrain. Ann NY Acad Sci 1016: 222-245, 2004.
61. Theunissen FE, David SV, Singh NC, Hsu A, Vinje WE, Gallant JL. Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli. Network 12: 289-316, 2001.
62. Vates GE, Broome BM, Mello CV, Nottebohm F. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J Comp Neurol 366: 613-642, 1996.
63. Wang L, Narayan R, Graña G, Shamir M, Sen K. Cortical discrimination of complex natural stimuli: can single neurons match behavior? J Neurosci 27: 582-589, 2007.
64. Wehr MS, Zador AM. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442-446, 2003.
65. Wilczynski W, Capranica RR. The auditory system of anuran amphibians. Prog Neurobiol 22: 1-38, 1984.
66. Wild JM, Karten HJ, Frost BJ. Connections of the auditory forebrain in the pigeon (Columba livia). J Comp Neurol 337: 32-62, 1993.
67. Woolley SMN, Fremouw TE, Hsu A, Theunissen FE. Tuning for spectrotemporal modulations as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 8: 1371-1379, 2005.
68. Zaraza DG, Margoliash D. The population representation of auditory objects rapidly expands and then contracts during learning. Soc Neurosci Abstr 33: 403.3, 2007.
69. Zeileis A. Econometric computing with HC and HAC covariance matrix estimators. J Stat Soft 11: 1-17, 2004.
70. Zoccolan D, Kouh M, Poggio T, DiCarlo JJ. Trade-off between object selectivity and tolerance in monkey inferotemporal cortex. J Neurosci 27: 12292-12307, 2007.