Behavioral relevance helps untangle natural vocal categories in a specific subset of core auditory cortical pyramidal neurons

Journal of Neuroscience

Volumn 35, Issue 6, 2015, Pages 2636-2645

  Shepard, Kathryn N ^a   Lin, Frank G ^b   Zhao, Charles L ^b   Chong, Kelly K ^b   Liu, Robert C ^a  

^a EMORY UNIVERSITY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Auditory object; Categorization; Communication; Map plasticity; Neural coding; Ultrasonic vocalization

Indexed keywords

ACOUSTIC NERVE FIBER; ADULT; ANIMAL COMMUNICATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY CORTEX; AUDITORY DISCRIMINATION; AUDITORY STIMULATION; CONTROLLED STUDY; CRANIOTOMY; CUB; ELECTROPHYSIOLOGICAL PROCEDURES; EVOKED AUDITORY RESPONSE; FEMALE; MOTHER; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NERVE POTENTIAL; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SIGNAL NOISE RATIO; SOUND TRANSMISSION; ULTRASOUND; VOCALIZATION; ANIMAL; ANIMAL BEHAVIOR; CBA MOUSE; CYTOLOGY; HEARING; PHYSIOLOGY;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; BEHAVIOR, ANIMAL; FEMALE; HEARING; MICE; MICE, INBRED CBA; NEURONAL PLASTICITY; PYRAMIDAL CELLS; SIGNAL-TO-NOISE RATIO; ULTRASONICS; VOCALIZATION, ANIMAL;

EID: 84922496543     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3803-14.2015     Document Type: Article

References (55)

1. Atencio CA, Schreiner CE (2008) Spectrotemporal processing differences between auditory cortical fast-spiking and regular-spiking neurons. J Neurosci 28: 3897-3910. CrossRef Medline.
2. Atencio CA, Sharpee TO, Schreiner CE (2008) Cooperative nonlinearities in auditory cortical neurons. Neuron 58: 956-966. CrossRef Medline.
3. Bao S, Chang EF, Teng CL, Heiser MA, Merzenich MM (2013) Emergent categorical representation of natural, complex sounds resulting from the early post-natal sound environment. Neuroscience 248: 30-42. CrossRef Medline.
4. Chang EF, Rieger JW, Johnson K, Berger MS, Barbaro NM, Knight RT (2010) Categorical speech representation in human superior temporal gyrus. Nat Neurosci 13: 1428-1432. CrossRef Medline.
5. Cohen L, Rothschild G, Mizrahi A (2011) Multisensory integration of natural odors and sounds in the auditory cortex. Neuron 72: 357-369. CrossRef Medline.
6. DiCarlo JJ, Zoccolan D, Rust NC (2012) How does the brain solve visual object recognition? Neuron 73: 415-434. CrossRef Medline.
7. DiMattina C, Wang X (2006) Virtual vocalization stimuli for investigating neural representations of species-specific vocalizations. J Neurophysiol 95: 1244-1262. CrossRef Medline.
8. Ehret G (1992) Categorical perception of mouse-pup ultrasounds in the temporal domain. Anim Behav 43: 409-416. CrossRef.
9. Ehret G, Haack B (1982) Ultrasound recognition in house mice: keystimulus configuration and recognition mechanism. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 148: 245-251. CrossRef.
10. Ehret G, Koch M (1989) Ultrasound-induced parental behavior in house mice is controlled by female sex-hormones and parental experience. Ethology 80: 81-93.
11. Ehret G, Koch M, Haack B, Markl H (1987) Sex and parental experience determine the onset of an instinctive behavior in mice. Naturwissenschaften 74: 47. CrossRef Medline.
12. Froemke RC, Merzenich MM, Schreiner CE (2007) A synaptic memory trace for cortical receptive field plasticity. Nature 450: 425-429. CrossRef Medline.
13. Froemke RC, Carcea I, Barker AJ, Yuan K, Seybold BA, Martins AR, Zaika N, Bernstein H, Wachs M, Levis PA, Polley DB, Merzenich MM, Schreiner CE (2013) Long-term modification of cortical synapses improves sensory perception. Nat Neurosci 16: 79-88. CrossRef Medline.
14. Galindo-Leon EE, Lin FG, Liu RC (2009) Inhibitory plasticity in a lateral band improves cortical detection of natural vocalizations. Neuron 62: 705-716. CrossRef Medline.
15. Gifford GW 3rd, MacLean KA, Hauser MD, Cohen YE (2005) The neurophysiology of functionally meaningful categories: macaque ventrolateral prefrontal cortex plays a critical role in spontaneous categorization of species-specific vocalizations. J Cogn Neurosci 17: 1471-1482. CrossRef Medline.
16. González-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA (2005) Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93: 942-953. CrossRef Medline.
17. Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J (2009) Female mice respond to male ultrasonic 'songs' with approach behaviour. Biol Lett 5: 589-592. CrossRef Medline.
18. Huetz C, Philibert B, Edeline JM (2009) A spike-timing code for discriminating conspecific vocalizations in the thalamocortical system of anesthetized and awake guinea pigs. J Neurosci 29: 334-350. CrossRef Medline.
19. Leaver AM, Rauschecker JP (2010) Cortical representation of natural complex sounds: effects of acoustic features and auditory object category. J Neurosci 30: 7604-7612. CrossRef Medline.
20. Li L, Xiong XR, Ibrahim LA, Yuan W, TaoHW, Zhang LI (2014) Differential receptive field properties of parvalbumin and somatostatin inhibitory neurons in mouse auditory cortex. Cereb Cortex. Advance online publication. Retrieved January 7, 2014. doi: 10. 1093/cercor/bht417. CrossRef Medline.
21. Lin FG, Liu RC (2010) Subset of thin spike cortical neurons preserve the peripheral encoding of stimulus onsets. J Neurophysiol 104: 3588-3599. CrossRef Medline.
22. Lin FG, Galindo-Leon EE, Ivanova TN, Mappus RC, Liu RC (2013) A role for maternal physiological state in preserving auditory cortical plasticity for salient infant calls. Neuroscience 247: 102-116. CrossRef Medline.
23. Liu RC (2006) Prospective contributions of transgenic mouse models to central auditory research. Brain Res 1091: 217-223. CrossRef Medline.
24. Liu RC, Schreiner CE (2007) Auditory cortical detection and discrimination correlates with communicative significance. PLoS Biol 5: e173. CrossRef Medline.
25. Liu RC, Miller KD, Merzenich MM, Schreiner CE (2003) Acoustic variability and distinguishability among mouse ultrasound vocalizations. J Acoust Soc Am 114: 3412-3422. CrossRef Medline.
26. Liu RC, Linden JF, Schreiner CE (2006) Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. Eur J Neurosci 23: 3087-3097. CrossRef Medline.
27. Margoliash D, Fortune ES (1992) Temporal and harmonic combinationsensitive neurons in the zebra finch's HVc. J Neurosci 12: 4309-4326. Medline.
28. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782-806. Medline.
29. Murray MM, Camen C, Gonzalez Andino SL, Bovet P, Clarke S (2006) Rapid brain discrimination of sounds of objects. J Neurosci 26: 1293-1302. CrossRef Medline.
30. Narayan R, Grana G, Sen K (2006) Distinct timescales in cortical discrimination of natural sounds in songbirds. J Neurophysiol 96: 252-258. CrossRef Medline.
31. Neubauer H, Heil P (2008) A physiological model for the stimulus dependence of first-spike latency of auditory-nerve fibers. Brain Res 1220: 208-223. CrossRef Medline.
32. Ohl FW, Scheich H, Freeman WJ (2001) Change in pattern of ongoing cortical activity with auditory category learning. Nature 412: 733-736. CrossRef Medline.
33. Polley DB, Steinberg EE, MerzenichMM (2006) Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci 26: 4970-4982. CrossRef Medline.
34. 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. CrossRef Medline.
35. Rauschecker JP, Tian B, HauserM (1995) Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268: 111-114. CrossRef Medline.
36. Recanzone GH, Schreiner CE, Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 13: 87-103. Medline.
37. Reed A, Riley J, Carraway R, Carrasco A, Perez C, Jakkamsetti V, Kilgard MP (2011) Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 70: 121-131. CrossRef Medline.
38. Rothschild G, Cohen L, Mizrahi A, Nelken I (2013) Elevated correlations in neuronal ensembles of mouse auditory cortex following parturition. J Neurosci 33: 12851-12861. CrossRef Medline.
39. Sadagopan S, Wang X (2009) Nonlinear spectrotemporal interactions underlying selectivity for complex sounds in auditory cortex. J Neurosci 29: 11192-11202. CrossRef Medline.
40. Schneider DM, Woolley SM (2013) Sparse and background-invariant coding of vocalizations in auditory scenes. Neuron 79: 141-152. CrossRef Medline.
41. Schreiner CE, Polley DB (2014) Auditory map plasticity: diversity in causes and consequences. Curr Opin Neurobiol 24: 143-156. CrossRef Medline.
42. Seger CA, Miller EK (2010) Category learning in the brain. Annu Rev Neurosci 33: 203-219. CrossRef Medline.
43. Shepard KN, Liu RC (2011) Experience restores innate female preference for male ultrasonic vocalizations. Genes Brain Behav 10: 28-34. CrossRef Medline.
44. Shepard KN, Kilgard MP, Liu RC (2012) Experience-dependent plasticity and the auditory cortex. In: Neural correlates of auditory cognition (Cohen YE, Popper AN, Fay RR, eds), pp 293-327. New York: Springer.
45. Stiebler I, Neulist R, Fichtel I, Ehret G (1997) The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation. J Comp Physiol A 181: 559-571. CrossRef Medline.
46. Suga N, O'Neill WE, Kujirai K, Manabe T (1983) Specificity of combinationsensitive neurons for processing of complex biosonar signals in auditory cortex of the mustached bat. J Neurophysiol 49: 1573-1626. Medline.
47. Thorpe S, Fize D, Marlot C (1996) Speed of processing in the human visual system. Nature 381: 520-522. CrossRef Medline.
48. Treue S (2003) Visual attention: the where, what, how and why of saliency. Curr Opin Neurobiol 13: 428-432. CrossRef Medline.
49. Tsao DY, Livingstone MS (2008) Mechanisms of face perception. Annu Rev Neurosci 31: 411-437. CrossRef Medline.
50. van Rossum MC (2001) A novel spike distance. Neural Comput 13: 751-763. CrossRef Medline.
51. Victor JD, Purpura KP (1997) Metric-space analysis of spike trains: theory, algorithms and application. Network Comp Neural 8: 127-164. CrossRef.
52. Wehr M, ZadorAM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442-446. CrossRef Medline.
53. Wehr M, ZadorAM (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47: 437-445. CrossRef Medline.
54. WeinbergerNM (2004) Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5: 279-290. CrossRef Medline.
55. Wu GK, Arbuckle R, Liu BH, Tao HW, Zhang LI (2008) Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58: 132-143. CrossRef Medline.