Selective and Efficient Neural Coding of Communication Signals Depends on Early Acoustic and Social Environment

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Amin, Noopur ^a   Gastpar, Michael ^b   Theunissen, Frédéric E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC ANALYSIS; ACOUSTIC STRESS; ANIMAL CELL; ANIMAL COMMUNICATION; ANIMAL TISSUE; ARTICLE; AUDITORY DISCRIMINATION; AUDITORY LATERALIZATION; AUDITORY STIMULATION; CONTROLLED STUDY; FEMALE; FINCH; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIMARY AUDITORY CORTEX; RECEPTIVE FIELD; SENSORY SYSTEM ELECTROPHYSIOLOGY; SOCIAL ENVIRONMENT; SOCIAL ISOLATION; SOUND DETECTION; SOUND TRANSMISSION; SPIKE WAVE; VOCALIZATION;

ACOUSTIC STIMULATION; ACOUSTICS; ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; FEMALE; FINCHES; MALE; MODELS, NEUROLOGICAL; SOCIAL ENVIRONMENT; VOCALIZATION, ANIMAL;

TAENIOPYGIA GUTTATA;

EID: 84876442330     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061417     Document Type: Article

References (70)

1. Rieke F, Bodnar DA, Bialek W, (1995) Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc Biol Sci 262: 259-65.
2. Lewicki MS, (2002) Efficient coding of natural sounds. Nat Neurosci 5: 356-63.
3. Machens CK, Gollisch T, Kolesnikova O, Herz AV, (2005) Testing the efficiency of sensory coding with optimal stimulus ensembles. Neuron 47: 447-56.
4. Smith EC, Lewicki MS, (2006) Efficient auditory coding. Nature 439: 978-82.
5. Escabí MA, Miller LM, Read HL, Schreiner CE, (2003) Naturalistic auditory contrast improves spectrotemporal coding in the cat inferior colliculus. J Neurosci 23: 11489-504.
6. Woolley SM, Fremouw TE, Hsu A, Theunissen FE, (2005) Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 8: 1371-9.
7. Garcia-Lazaro JA, Ahmed B, Schnupp JW, (2006) Tuning to natural stimulus dynamics in primary auditory cortex. Curr Biol 16: 264-71.
8. Wollberg Z, Newman JD, (1972) Auditory cortex of squirrel monkey: response patterns of single cells to species-specific vocalizations. Science 175: 212-4.
9. Wang X, Merzenich MM, Beitel R, Schreiner CE, (1995) Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J Neurophysiol 74: 2685-706.
10. Tian B, Reser D, Durham A, Kustov A, Rauschecker JP, (2001) Functional specialization in rhesus monkey auditory cortex. Science 292: 290-3.
11. Kilgard MP, Merzenich MM, (1998) Plasticity of temporal information processing in the primary auditory cortex. Nat Neurosci 1: 721-731.
12. Zhang LI, Bao S, Merzenich MM, (2001) Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 4: 123-30.
13. Chang EF, Merzenich MM, (2003) Environmental noise retards auditory cortical development. Science 300: 498-502.
14. Chang EF, Bao S, Imaizumi K, Schreiner CE, Merzenich MM, (2005) Development of spectral and temporal response selectivity in the auditory cortex. Proc Natl Acad Sci 102: 16460-5.
15. Han YK, Kover H, Insanally MN, Semerdjian JH, Bao S, (2007) Early experience impairs perceptual discrimination. Nat Neurosci 10: 1191-1197.
16. Zhou X, Merzenich MM, (2008) Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex. Proc Natl Acad Sci 105: 4423-8.
17. Zhou X, Panizzutti R, de Villers-Sidani E, Madeira C, Merzenich MM, (2011) Natural restoration of critical period plasticity in the juvenile and adult primary auditory cortex. J Neurosci 31: 5625-5634.
18. Thorpe WH, (1958) The learning of song patterns by birds with especial reference to the song of the chaffinch, Fringilla coelebs. Ibis 100: 535-70.
19. Marler P, (1970) A comparative approach to vocal learning: song development in white-crowned sparrows. J Comp Physiol Psychol 71: 1-25.
20. Doupe AJ, Kuhl PK, (1999) Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22: 567-631.
21. Theunissen FE, Amin N, Shaevitz SS, Woolley SM, Fremouw T, et al. (2004) Song selectivity in the song system and in the auditory forebrain. Ann N Y Acad Sci 1016: 222-45.
22. Gentner TQ, Margoliash D, (2003) Neuronal populations and single cells representing learned auditory objects. Nature 424: 669-74.
23. Cousillas H, Richard JP, Mathelier M, Henry L, George I, et al. (2004) Experience-dependent neuronal specialization and functional organization in the central auditory area of a songbird. Eur J Neurosci 19: 3343-3352.
24. Phan ML, Pytte CL, Vicario DS, (2006) Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc Natl Acad Sci U S A 103: 1088-1093.
25. Keller GB, Hahnloser RH, (2009) Neural processing of auditory feedback during vocal practice in a songbird. Nature 457: 187-190.
26. Grace JA, Amin N, Singh NC, Theunissen FE, (2003) Selectivity for conspecific song in the zebra finch auditory forebrain. J Neurophysiol 89: 472-487.
27. Amin N, Doupe A, Theunissen FE, (2007) Development of selectivity for natural sounds in the songbird auditory forebrain. J Neurophysiol 97: 3517-31.
28. Hsu A, Woolley SM, Fremouw TE, Theunissen FE, (2004) Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons. J Neurosci 24: 9201-11.
29. Cynx J, Lewis R, Tavel B, Tse H, (1998) Amplitude regulation of vocalizations in noise by a songbird, Taeniopygia guttata. Anim Behav 56: 107-113.
30. Ryals BM, Dooling RJ, Westbrook E, Dent ML, MacKenzie A, et al. (1999) Avian species differences in susceptibility to noise exposure. Hear Res 1131: 71-88.
31. Zevin JD, Seidenberg MS, Bottjer SW, (2004) Limits on reacquisition of song in adult zebra finches exposed to white noise. J Neurosci 24: 5849-62.
32. Funabiki Y, Konishi M, (2003) Long memory in song learning by zebra finches. J Neurosci 23: 6928-35.
33. Woolley SM, Gill PR, Fremouw T, Theunissen FE, (2009) Functional groups in the avian auditory system. J Neurosci 29: 2780-93.
34. Fortune ES, Margoliash D, (1992) Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (Taenopygia guttata). J Comp Neurol 325: 388-404.
35. Theunissen FE, Sen K, Doupe AJ, (2000) Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J Neurosci 20: 2315-2331.
36. Gill P, Zhang J, Woolley SM, Fremouw T, Theunissen FE, (2006) Sound representation methods for spectro-temporal receptive field estimation. J Comput Neurosci 21: 5-20.
37. Strong SP, Koberle R, de Ruyter van Steveninck RR, Bialek W, (1998) Entropy and information in neural spike trains. Phys Rev Lett 80: 197-200.
38. Wang L, Narayan R, Graña G, Shamir M, Sen K, (2007) Cortical discrimination of complex natural stimuli: can single neurons match behavior? J Neurosci 27: 582-9.
39. Gastpar MC, Gill PR, Huth AG, Theunissen FE, (2010) Anthropic correction of information estimates and its application to neural coding. IEEE Transactions on Information Theory 56: 890-900.
40. Wang Y, Brzozowska-Prechti A, Karten HJ, (2010) Laminar and columnar auditory cortex in avian brain. PNAS 107 (28) (): 12676-12681.
41. Gao F, Zhang J, Sun X, Chen L, (2009) The effect of postnatal exposure to noise on sound level processing by auditory cortex neurons of rats in adulthood. Physiol Behav 97: 369-73.
42. Hogsden JL, Dringenberg HC, (2009) NR2B subunit-dependent long-term potentiation enhancement in the rat cortical auditory system in vivo following masking of patterned auditory input by white noise exposure during early postnatal life. Eur J Neurosci 30: 376-84.
43. Xu J, Yu L, Cai R, Zhang J, Sun X, (2010) Early continuous white noise exposure alters auditory spatial sensitivity and expression of GAD65 and GABAA receptor subunits in rat auditory cortex. Cereb Cortex 20: 804-12.
44. de Villers-Sidani E, Simpson KL, Lu YF, Lin RC, Merzenich MM, (2008) Manipulating critical period closure across different sectors of the primary auditory cortex. Nat Neurosci 11: 957-65.
45. Wild MJ, Karten HJ, Frost BJ, (1993) Connections of the auditory forebrain in the pigeon (columba livia). J Comp Neurol 337: 32-62.
46. Vates GE, Broome BM, Mello CV, Nottebohm F, (1996) Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata). J Comp Neurol 366: 613-642.
47. Albus K, Wolf W, (1984) Early post-natal development of neuronal function in the kitten's visual cortex: a laminar analysis. J Physiol 348: 153-185.
48. Fox K, (1992) A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci 12 (5) (): 1826-1838.
49. Wiesel TN, Hubel DH, (1974) Ordered arrangement of orientation columns in monkeys lacking visual experience. J Comp Neurol 158 (3) (): 307-318.
50. Godecke I, Bonhoeffer T, (1996) Development of identical orientation maps for two eyes without common visual experience. Nature 379: 251-254.
51. Crair MC, Gillespie DC, Stryker MP, (1998) The role of visual experience in the development of columns in cat visual cortex. Science 279 (5350) (): 566-570.
52. Caspary DM, Ling L, Turner JG, Hughes LF, (2008) Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exptl Biol 211: 1781-1791.
53. Celikel T, Szostak VA, Feldman DE, (2004) Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci 7: 534-541.
54. Cassenaer S, Laurent G, (2007) Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448: 709-713.
55. Jun JK, Jin DZ, (2007) Development of neural circuitry for precise temporal sequences through spontaneous activity, axon remodeling, and synaptic plasticity. PLoS ONE 2: e723.
56. Talathi SS, Hwang D, Ditto WL, (2008) Spike timing dependent plasticity promotes synchrony of inhibitory networks in the presence of heterogeneity. J Comput Neurosci 25: 262-281.
57. Fiete IR, Senn W, Wang CZ, Hahnloser RH, (2010) Spike-timing dependent plasticity and heterosynaptic competition organize networks to produce long scale-free sequences of neural activity. Neuron 65: 563-576.
58. Boettiger CA, Doupe AJ, (2001) Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron 31: 809-818.
59. Ding L, Perkel DJ, (2004) Long-term potentiation in an avian basal ganglia nucleus essential for vocal learning. J Neurosci 24: 488-494.
60. Rosen MJ, Mooney R, (2003) Inhibitory and excitatory mechanisms underlying auditory responses to learned vocalizations in the songbird nucleus HVC. Neuron 39: 177-194.
61. Pinaud R, Terleph TA, Tremere LA, Phan ML, Dagostin AA, et al. (2008) Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain. J Neurophysiol 100: 441-455.
62. Olshausen BA, Field DJ, (2004) Sparse coding of sensory inputs. Curr Opin Neurobiol 14: 481-7.
63. Blattler F, Hahnloser RH, (2011) An efficient coding hypothesis links sparsity and selectivity of neural responses. PLoS ONE 6: e25506.
64. Olshausen BA, Field DJ, (1996) Emergence of simple cell receptive field properties by learning a sparse code for natural images. Nature 381: 607-609.
65. Willmore B, Tolhurst DJ, (2001) Characterizing the sparseness of neural codes. Network 12: 255-270.
66. Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, et al. (2002) Oscillations and sparsening of odor representations in the mushroom body. Science 297: 359-365.
67. Vinje WE, Gallant JL, (2002) Natural stimulation of the nonclassical receptive field increases information transmission efficiency in V1. J Neurosci 22: 2904-2915.
68. Chechik G, Anderson MJ, Bar-Yosef O, Young ED, Tishby N, et al. (2006) Reduction of information redundancy in the ascending auditory pathway. Neuron 51: 359-68.
69. Billimoria CP, Kraus BJ, Narayan R, Maddox RK, Sen K, (2008) Invariance and sensitivity to intensity in neural discrimination of natural sounds. J Neurosci 28: 6304-8.
70. Hromádka T, Deweese MR, Zador AM, (2008) Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol 6: e16.