Emergence of learned categorical representations within an auditory forebrain circuit

Journal of Neuroscience

Volumn 31, Issue 7, 2011, Pages 2595-2606

  Jeanne, James M ^a,b   Thompson, Jason V ^a   Sharpee, Tatyana O ^a,b   Gentner, Timothy Q ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; BRAIN NERVE CELL; CAUDOLATERAL MESOPALLIUM; CONTROLLED STUDY; FOREBRAIN; LEARNING; MALE; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SINGLE UNIT ACTIVITY; STARLING;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY PERCEPTION; LEARNING; NERVE NET; NEURONS; PROBABILITY; PROSENCEPHALON; RECOGNITION (PSYCHOLOGY); STARLINGS; STATISTICS, NONPARAMETRIC; VOCALIZATION, ANIMAL;

EID: 79951815608     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3930-10.2011     Document Type: Article

References (62)

1. Amin N, Grace JA, Theunissen FE (2004) Neural response to bird's own song and tutor song in the zebra finch field L and caudal mesopallium. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:469-489. (Pubitemid 40876379)
2. Asari H, Zador AM (2009) Long-lasting context dependence constrains neural encoding models in rodent auditory cortex. J Neurophysiol 102:2638-2656.
3. Bauer EE, Coleman MJ, Roberts TF, Roy A, Prather JF, Mooney R (2008) A synaptic basis for auditory-vocal integration in the songbird. J Neurosci 28:1509-1522. (Pubitemid 351231533)
4. Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Springer JA, Kaufman JN, Possing ET (2000) Human temporal lobe activation by speech and non-speech sounds. Cereb Cortex 10:512-528. (Pubitemid 30318458)
5. Blake DT, Heiser MA, Caywood M, Merzenich MM (2006) Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward. Neuron 52:371-381. (Pubitemid 44548340)
6. Bonke D, Scheich H, Langner G (1979) Responsiveness of units in the auditory neostriatum of the guinea fowl (Numida meleagris) to species-specific calls and synthetic stimuli. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 132:243-255.
7. Brenner N, Strong SP, Koberle R, Bialek W, de Ruyter van Steveninck RR (2000) Synergy in a neural code. Neural Comput 12:1531-1552.
8. Chaiken M, Böhner J, Marler P (1993) Song acquisition in European starlings, Sturnus vulgaris: a comparison of the songs of live-tutored, tape-tutored, untutored, and wild-caught males. Anim Behav 46:1079-1090.
9. Chechik G, Anderson MJ, Bar-Yosef O, Young ED, Tishby N, Nelken I (2006) Reduction of information redundancy in the ascending auditory pathway. Neuron 51:359-368. (Pubitemid 44118713)
10. Cover T, Thomas J (2006) Elements of information theory, Ed 2. Hoboken, NJ: Wiley.
11. Desimone R, Albright TD, Gross CG, Bruce C (1984) Stimulus-selective properties of inferior temporal neurons in the macaque. J Neurosci 4:2051-2062. (Pubitemid 14025567)
12. Eens M (1997) Understanding the complex song of the European starling: an integrated ethological approach. Adv Study Behav 26:355-434.
13. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47.
14. Franco L, Rolls ET, Aggelopoulos NC, Jerez JM (2007) Neuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex. Biol Cybern 96:547-560. (Pubitemid 46835373)
15. Freedman DJ, Assad JA (2006) Experience-dependent representation of visual categories in parietal cortex. Nature 443:85-88. (Pubitemid 44344052)
16. Freedman DJ, Miller EK (2008) Neural mechanisms of visual categorization: insights from neurophysiology. Neurosci Biobehav Rev 32:311-329.
17. Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2001) Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291:312-316. (Pubitemid 32096318)
18. Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2003) A comparison of primate prefrontal and inferior temporal cortices during visual categorization. J Neurosci 23:5235-5246. (Pubitemid 36793252)
19. Gentner TQ (2008) Temporal scales of auditory objects underlying birdsong vocal recognition. J Acoust Soc Am 124:1350-1359.
20. Gentner TQ, Hulse SH (2000) Perceptual classification based on the component structure of song in European starlings. J Acoust Soc Am 107:3369-3381. (Pubitemid 30397031)
21. Gentner TQ, Margoliash D (2003) Neuronal populations and single cells representing learned auditory objects. Nature 424:669-674. (Pubitemid 36987990)
22. Gill P, Woolley SM, Fremouw T, Theunissen FE (2008) What's that sound? Auditory area CLM encodes stimulus surprise, not intensity or intensity changes. J Neurophysiol 99:2809-2820.
23. Hoffman KL, Logothetis NK (2009) Cortical mechanisms of sensory learning and object recognition. Philos Trans R Soc Lond B Biol Sci 364:321-329.
24. 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 24:9201-9211. (Pubitemid 39372264)
25. Janata P, Margoliash D (1999) Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J Neurosci 19:5108-5118. (Pubitemid 29270145)
26. Kaas JH, Hackett TA (2000) Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci U S A 97:11793-11799.
27. Kikuchi Y, Horwitz B, Mishkin M (2010) Hierarchical auditory processing directed rostrally along the monkey's supratemporal plane. J Neurosci 30:13021-13030.
28. Langner G, Bonke D, Scheich H (1981) Neuronal discrimination of natural and synthetic vowels in field L of trained mynah birds. Exp Brain Res 43:11-24. (Pubitemid 11064803)
29. Lehky SR, Sejnowski TJ, Desimone R (2005) Selectivity and sparseness in the responses of striate complex cells. Vision Res 45:57-73. (Pubitemid 39574758)
30. Macmillan NA, Creelman CD (2005) Detection theory, a user's guide. Mahwah, NJ: Lawrence Erlbaum Associates.
31. Margoliash D (1983) Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J Neurosci 3:1039-1057.
32. Maunsell JH, Newsome WT (1987) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363-401. (Pubitemid 17022778)
33. Meliza CD, Chi Z, Margoliash D (2010) Representations of conspecific song by starling secondary forebrain auditory neurons: toward a hierarchical framework. J Neurophysiol 103:1195-1208.
34. Merzenich MM, deCharms RC (1996) Neural representations, experience, and change. In: The mind-brain continuum (Llinas R, Churchland PS, eds), pp 61-81. Cambridge, MA: MIT.
35. Messinger A, Squire LR, Zola SM, Albright TD (2001) Neuronal representations of stimulus associations develop in the temporal lobe during learning. Proc Natl Acad Sci U S A 98:12239-12244. (Pubitemid 32959857)
36. Nahum M, Nelken I, Ahissar M (2008) Low-level information and high-level perception: the case of speech in noise. PLoS Biol 6:e126.
37. Nelken I (2004) Processing of complex stimuli and natural scenes in the auditory cortex. Curr Opin Neurobiol 14:474-480.
38. Panzeri S, Senatore R, Montemurro MA, Petersen RS (2007) Correcting for the sampling bias problem in spike train information measures. J Neurophysiol 98:1064-1072. (Pubitemid 47435863)
39. Pinaud R, Velho TA, Jeong JK, Tremere LA, Leão RM, von Gersdorff H, Mello CV (2004) GABAergic neurons participate in the brain's response to birdsong auditory stimulation. Eur J Neurosci 20:1318-1330. (Pubitemid 39233583)
40. Polley DB, Steinberg EE, Merzenich MM (2006) Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci 26:4970-4982. (Pubitemid 44315340)
41. Prather JF, Nowicki S, Anderson RC, Peters S, Mooney R (2009) Neural correlates of categorical perception in learned vocal communication. Nat Neurosci 12:221-228.
42. Rauschecker JP, Scott SK (2009) Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12:718-724.
43. Riesenhuber M, Poggio T (2000) Models of object recognition. Nat Neurosci 3 [Suppl]:1199-1204.
44. Rolls ET, Tovee MJ (1995) Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J Neurophysiol 73:713-726.
45. Rolls ET, Baylis GC, Hasselmo ME, Nalwa V (1989) The effect of learning on the face selective responses of neurons in the cortex in the superior temporal sulcus of the monkey. Exp Brain Res 76:153-164. (Pubitemid 19167227)
46. Russ BE, Ackelson AL, Baker AE, Cohen YE (2008) Coding of auditory-stimulus identity in the auditory non-spatial processing stream. J Neurophysiol 99:87-95.
47. Rust NC, DiCarlo JJ (2010) Selectivity and tolerance (" invariance") both increase as visual information propagates from cortical area V4 to IT. J Neurosci 30:12978-12995.
48. Seeba F, Klump GM (2009) Stimulus familiarity affects perceptual restoration in the European starling (Sturnus vulgaris). PLoS One 4:e5974.
49. Seger CA, Miller EK (2010) Category learning in the brain. Annu Rev Neurosci 33:203-219.
50. Sen K, Theunissen FE, Doupe AJ (2001) Feature analysis of natural sounds in the songbird auditory forebrain. J Neurophysiol 86:1445-1458. (Pubitemid 32847788)
51. Shaevitz SS, Theunissen FE (2007) Functional connectivity between auditory areas field L and CLM and song system nucleus HVC in anesthetized zebra finches. J Neurophysiol 98:2747-2764. (Pubitemid 350127935)
52. Sigala N, Logothetis NK (2002) Visual categorization shapes feature selectivity in the primate temporal cortex. Nature 415:318-320. (Pubitemid 34087552)
53. 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. (Pubitemid 128621483)
54. Thompson JV, Gentner TQ (2010) Song recognition learning and stimulus-specific weakening of neural responses in the avian auditory forebrain. J Neurophysiol 103:1785-1797.
55. Treves A, Panzeri S (1995) The upward bias in measures of information derived from limited data samples. Neural Comput 7:399-407.
56. Van Essen DC, Anderson CH, Felleman DJ (1992) Information processing in the primate visual system: an integrated systems perspective. Science 255:419-423.
57. 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. J Comp Neurol 366:613-642. (Pubitemid 26087298)
58. Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273-1276. (Pubitemid 30112150)
59. Willmore B, Tolhurst DJ (2001) Characterizing the sparseness of neural codes. Network 12:255-270. (Pubitemid 33626946)
60. Winer JA, Miller LM, Lee CC, Schreiner CE (2005) Auditory thalamocortical transformation: structure and function. Trends Neurosci 28:255-263. (Pubitemid 41556910)
61. 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 8:1371-1379. (Pubitemid 41630426)
62. Woolley SM, Gill PR, Fremouw T, Theunissen FE (2009) Functional groups in the avian auditory system. J Neurosci 29:2780-2793.