Emergence of invariant representation of vocalizations in the auditory cortex

Journal of Neurophysiology

Volumn 114, Issue 5, 2015, Pages 2726-2740

  Carruthers, Isaac M ^a   Laplagne, Diego A ^b   Jaegle, Andrew ^a   Briguglio, John J ^a   Mwilambwe Tshilobo, Laetitia ^a   Natan, Ryan G ^a,b   Geffen, Maria N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

Author keywords

Auditory cortex; Hierarchical coding; Invariance; Processing; Vocalizations

Indexed keywords

ADULT; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY SYSTEM; FREQUENCY MODULATION; MALE; NERVE POTENTIAL; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; PURE TONE AUDIOMETRY; RAT; SOCIAL INTERACTION; SUPPORT VECTOR MACHINE; VOCALIZATION; ACTION POTENTIAL; ANIMAL; HEARING; LONG EVANS RAT; NERVE CELL; PHYSIOLOGY; SOUND DETECTION;

ACTION POTENTIALS; ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; MALE; NEURONS; RATS; RATS, LONG-EVANS; SOUND SPECTROGRAPHY; VOCALIZATION, ANIMAL;

EID: 84947286361     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00095.2015     Document Type: Article

References (92)

1. Abbott LF. Decoding neuronal firing and modelling neural networks. Q Rev Biophys 27: 291–331, 1994.
2. Aizenberg M, Geffen MN. Bidirectional effects of auditory aversive learning on sensory acuity are mediated by the auditory cortex. Nat Neurosci 16: 994–996, 2013.
3. Arnault P, Roger M. Ventral temporal cortex in the rat: connections of secondary auditory areas Te2 and Te3. J Comp Neurol 302: 110–123, 1990.
4. Asari H, Zador A. Long-lasting context dependence constrains neural encoding models in rodent auditory cortex. J Neurophysiol 102: 2638–2656, 2009.
5. Atencio C, Sharpee T, Schreiner C. Hierarchical computation in the canonical auditory cortical circuit. Proc Natl Acad Sci USA 106: 21894–21899, 2009.
6. Averbeck BB, Latham PE, Pouget A. Neural correlations, population coding and computation. Nat Rev Neurosci 7: 358–366, 2006.
7. Averbeck BB, Lee D. Coding and transmission of information by neural ensembles. Trends Neurosci 27: 225–230, 2004.
8. Barfield RJ, Auerbach P, Geyer LA, Mcintosh TK. Ultrasonic vocalizations in rat sexual-behavior. Am Zool 19: 469–480, 1979.
9. Beasley DS, Bratt GW, Rintelmann WF. Intelligibility of time-compressed sentential stimuli. J Speech Hear Res 23: 722–731, 1980.
10. Bialy M, Rydz M, Kaczmarek L. Precontact 50-kHz vocalizations in male rats during acquisition of sexual experience. Behav Neurosci 114: 983–990, 2000.
11. Bizley JK, Walker KM, Silverman BW, King AJ, Schnupp JW. Interdependent encoding of pitch, timbre, and spatial location in auditory cortex. J Neurosci 29: 2064–2075, 2009.
12. Blake DT, Merzenich MM. Changes of AI receptive fields with sound density. J Neurophysiol 88: 3409–3420, 2002.
13. Brudzynski SM. Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50: 43–50, 2009.
14. Brudzynski SM, Pniak A. Social contacts and production of 50-kHz short ultrasonic calls in adult rats. J Comp Psychol 116: 73–82, 2002.
15. Burgdorf J, Knutson B, Panksepp J. Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behavioral Neurosci 114: 320–327, 2000.
16. Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J. Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and selfadministration of playback. J Comp Psychol 122: 357–367, 2008.
17. Carrasco A, Lomber SG. Neuronal activation times to simple, complex, and natural sounds in cat primary and nonprimary auditory cortex. J Neurophysiol 106: 1166–1178, 2011.
18. Carruthers IM, Natan RG, Geffen MN. Encoding of ultrasonic vocalizations in the auditory cortex. J Neurophysiol 109: 1912–1927, 2013.
19. Chang CC, Lin CJ. LIBSVM: A Library for Support Vector Machines. Acm T Intel Syst Tec 2: 2011.
20. Cohen MR, Kohn A. Measuring and interpreting neuronal correlations. Nat Neurosci 14: 811–819, 2011.
21. Covic EN, Sherman SM. Synaptic properties of connections between the primary and secondary auditory cortices in mice. Cereb Cortex 21: 2425–2441, 2011.
22. Dayan P, Abbott LF. Theoretical Neuroscience Computational and Mathematical Modeling of Neural Systems. Cambridge, MA: MIT Press, 2005.
23. deCharms RC, Zador A. Neural representation and the cortical code. Annu Rev Neurosci 23: 613–647, 2000.
24. DiCarlo JJ, Cox DD. Untangling invariant object recognition. Trends Cogn Sci 11: 333–341, 2007.
25. Dupoux E, Green K. Perceptual adjustment to highly compressed speech: effects of talker and rate changes. J Exp Psychol Hum Percept Perform 23: 914–927, 1997.
26. Elie JE, Theunissen FE. Meaning in the avian auditory cortex: neural representation of communication calls. Eur J Neurosci 41: 546–567, 2015.
27. Engineer CT, Perez CA, Chen YH, Carraway RS, Reed AC, Shetake JA, Jakkamsetti V, Chang KQ, Kilgard MP. Cortical activity patterns predict speech discrimination ability. Nat Neurosci 11: 603–608, 2008.
28. Fitch RH, Miller S, Tallal P. Neurobiology of speech perception. Annu Rev Neurosci 20: 331–353, 1997.
29. Foulke E, Sticht TG. Review of research on the intelligibility and comprehension of accelerated speech. Psychol Bull 72: 50–62, 1969.
30. Fritz JB, David SV, Radtke-Schuller S, Yin P, Shamma SA. Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex. Nat Neurosci 13: 1011–1019, 2010.
31. Gai Y, Carney LH. Statistical analyses of temporal information in auditory brainstem responses to tones in noise: correlation index and spike-distance metric. J Assoc Res Otolaryngol 9: 373–387, 2008.
32. Galindo-Leon EE, Lin FG, Liu RC. Inhibitory plasticity in a lateral band improves cortical detection of natural vocalizations. Neuron 62: 705–716, 2009.
33. Gehr DD, Komiya H, Eggermont JJ. Neuronal responses in cat primary auditory cortex to natural and altered species-specific calls. Hear Res 150: 27–42, 2000.
34. Glass I, Wollberg Z. Responses of cells in the auditory cortex of awake squirrel monkeys to normal and reversed species-specific vocalizations. Hear Res 9: 27–33, 1983.
35. Holmstrom LA, Eeuwes LB, Roberts PD, Portfors CV. Efficient encoding of vocalizations in the auditory midbrain. J Neurosci 30: 802–819, 2010.
36. Huetz C, Philibert B, Edeline JM. A spike-timing code for discriminating conspecific vocalizations in the thalamocortical system of anesthetized and awake guinea pigs. J Neurosci 29: 334–350, 2009.
37. Hung CP, Kreiman G, Poggio T, DiCarlo JJ. Fast readout of object identity from macaque inferior temporal cortex. Science 310: 863–866, 2005.
38. Kaas JH, Hackett TA. Subdivisions of auditory cortex and levels of processing in primates. Audiol Neurootol 3: 73–85, 1998.
39. Kanold PO, Nelken I, Polley DB. Local versus global scales of organization in auditory cortex. Trends Neurosci 37: 502–510, 2014.
40. Kikuchi Y, Horwitz B, Mishkin M. Hierarchical auditory processing directed rostrally along the monkey’s supratemporal plane. J Neurosci 30: 13021–13030, 2010.
41. Kimura A, Donishi T, Sakoda T, Hazama M, Tamai Y. Auditory thalamic nuclei projections to the temporal cortex in the rat. Neuroscience 117: 1003–1016, 2003.
42. Knutson B, Burgdorf J, Panksepp J. Anticipation of play elicits highfrequency ultrasonic vocalizations in young rats. J Comp Psychol 112: 65–73, 1998.
43. Knutson B, Burgdorf J, Panksepp J. Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 128: 961–977, 2002.
44. Kusmierek P, Rauschecker JP. Functional specialization of medial auditory belt cortex in the alert rhesus monkey. J Neurophysiol 102: 1606–1622, 2009.
45. Kvale M, Schreiner C. Short-term adaptation of auditory receptive fields to dynamic stimuli. J Neurophysiol 91: 604–612, 2004.
46. Lakatos P, Pincze Z, Fu KM, Javitt DC, Karmos G, Schroeder CE. Timing of pure tone and noise-evoked responses in macaque auditory cortex. Neuroreport 16: 933–937, 2005.
47. LeDoux JE, Farb CR, Romanski LM. Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neurosci Lett 134: 139–144, 1991.
48. Liu RC, Linden JF, Schreiner CE. Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. Eur J Neurosci 23: 3087–3097, 2006.
49. Liu RC, Schreiner CE. Auditory cortical detection and discrimination correlates with communicative significance. PLoS Biol 5: e173, 2007.
50. Marlin BJ, Mitre M, D’Amour JA, Chao MV, Froemke RC. Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520: 499–504, 2015.
51. McIntosh TK, Barfield RJ, Geyer LA. Ultrasonic vocalisations facilitate sexual behaviour of female rats. Nature 272: 163–164, 1978.
52. Medvedev AV, Kanwal JS. Local field potentials and spiking activity in the primary auditory cortex in response to social calls. J Neurophysiol 92: 52–65, 2004.
53. Natan RG, Briguglio JJ, Mwilambwe-Tshilobo L, Jones S, Aizenberg M, Goldberg EM, Geffen MN. Complementary control of sensory adaptation by two types of cortical interneurons. eLife 2015: 10.7554/eLife.09868, 2015.
54. Otazu GH, Tai LH, Yang Y, Zador AM. Engaging in an auditory task suppresses responses in auditory cortex. Nat Neurosci 12: 646–654, 2009.
55. Parrott RF. Effect of castration on sexual arousal in the rat, determined from records of post-ejaculatory ultrasonic vocalizations. Physiol Behav 16: 689–692, 1976.
56. Paxinos G, Watson C. The Rat Brain in Stereotactic Coordinates. Sydney: Academic, 1986.
57. Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V, Vanderplas J, Passos A, Cournapeau D, Brucher M, Perrot M, Duchesnay E. Scikit-learn: Machine Learning in Python. J Mach Learn Res 12: 2825–2830, 2011.
58. Pelleg-Toiba R, Wollberg Z. Discrimination of communication calls in the squirrel monkey: “call detectors” or “cell ensembles”? J Basic Clin Physiol Pharmacol 2: 257–272, 1991.
59. Petkov CI, Kayser C, Augath M, Logothetis NK. Functional imaging reveals numerous fields in the monkey auditory cortex. PLoS Biol 4: e215, 2006.
60. Pincherli Castellanos TA, Aitoubah J, Molotchnikoff S, Lepore F, Guillemot JP. Responses of inferior collicular cells to species-specific vocalizations in normal and enucleated rats. Exp Brain Res 183: 341–350, 2007.
61. Polley DB, Read HL, Storace DA, Merzenich MM. Multiparametric auditory receptive field organization across five cortical fields in the albino rat. J Neurophysiol 97: 3621–3638, 2007.
62. Portfors CV. Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci 46: 28–34, 2007.
63. Profant O, Burianova J, Syka J. The response properties of neurons in different fields of the auditory cortex in the rat. Hear Res 296: 51–59, 2013.
64. Rabinowitz NC, Willmore BD, King AJ, Schnupp JW. Constructing noiseinvariant representations of sound in the auditory pathway. PLoS Biol 11: e1001710, 2013.
65. Rabinowitz NC, Willmore BD, Schnupp JW, King AJ. Contrast gain control in auditory cortex. Neuron 70: 1178–1191, 2011.
66. Rauschecker JP, Tian B. Processing of band-passed noise in the lateral auditory belt cortex of the rhesus monkey. J Neurophysiol 91: 2578–2589, 2004.
67. Rauschecker JP, Tian B, Hauser M. Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268: 111–114, 1995.
68. Recanzone GH, Cohen YE. Serial and parallel processing in the primate auditory cortex revisited. Behav Brain Res 206: 1–7, 2010.
69. Roger M, Arnault P. Anatomical study of the connections of the primary auditory area in the rat. J Comp Neurol 287: 339–356, 1989.
70. Romanski LM, LeDoux JE. Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cereb Cortex 3: 515–532, 1993a.
71. Romanski LM, LeDoux JE. Organization of rodent auditory cortex: anterograde transport of PHA-L from MGv to temporal neocortex. Cereb Cortex 3: 499–514, 1993b.
72. Rust NC, DiCarlo JJ. Balanced increases in selectivity and tolerance produce constant sparseness along the ventral visual stream. J Neurosci 32: 10170–10182, 2012.
73. Rust NC, Dicarlo JJ. Selectivity and tolerance (“invariance”) both increase as visual information propagates from cortical area V4 to IT. J Neurosci 30:12978–12995, 2010.
74. Rutkowski RG, Miasnikov AA, Weinberger NM. Characterisation of multiple physiological fields within the anatomical core of rat auditory cortex. Hear Res 181: 116–130, 2003.
75. Sales GD. Ultrasound and mating behavior in rodents with some observations on other behavioral situations. J Zool 68: 149–164, 1972.
76. Sally S, Kelly J. Organization of auditory cortex in the albino rat: sound frequency. J Neurophysiol 59: 1627–1638, 1988.
77. Schneider DM, Woolley SM. Discrimination of communication vocalizations by single neurons and groups of neurons in the auditory midbrain. J Neurophysiol 103: 3248–3265, 2010.
78. Schnupp JW, Hall TM, Kokelaar RF, Ahmed B. Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J Neurosci 26: 4785–4795, 2006.
79. Sewell GD. Ultrasonic communication in rodents. Nature 227: 410, 1970.
80. Sharpee T, Atencio C, Schreiner C. Hierarchical representations in the auditory cortex. Curr Opin Neurobiol 21: 761–767, 2011.
81. Sirotin YB, Costa ME, Laplagne DA. Rodent ultrasonic vocalizations are bound to active sniffing behavior. Front Behav Neurosci 8: 399, 2014.
82. Storace DA, Higgins NC, Read HL. Thalamic label patterns suggest primary and ventral auditory fields are distinct core regions. J Comp Neurol 518: 1630–1646, 2010.
83. Takahashi N, Kashino M, Hironaka N. Structure of rat ultrasonic vocalizations and its relevance to behavior. PLoS One 5: e14115, 2010.
84. Ulanovsky N, Las L, Farkas D, Nelken I. Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24: 10440–10453, 2004.
85. Vapnik V. The Nature of Statistical Learning. Springer Verlag, 2000.
86. Wallace MN, Shackleton TM, Anderson LA, Palmer AR. Representation of the purr call in the guinea pig primary auditory cortex. Hear Res 204: 115–126, 2005.
87. Wang X, Merzenich MM, Beitel R, Schreiner CE. Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J Neurophysiol 74: 2685–2706, 1995.
88. Winer JA, Kelly JB, Larue DT. Neural architecture of the rat medial geniculate body. Hear Res 130: 19–41, 1999.
89. Winer JA, Schreiner CE. The Auditory Cortex. New York: Springer, 2010.
90. Wohr M, Houx B, Schwarting RK, Spruijt B. Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93: 766–776, 2008.
91. Woolley S, Fremouw T, Hsu A, Theunissen F. Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 8: 1371–1379, 2005.
92. Wright JM, Gourdon JC, Clarke PB. Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context. Psychopharmacology 211: 1–13, 2010.