Level Invariant Representation of Sounds by Populations of Neurons in Primary Auditory Cortex

Overview

Journal J Neurosci

Specialty Neurology

Date 2008 Mar 28

PMID 18367608

Citations 84

Authors

Srivatsun Sadagopan

Xiaoqin Wang

Affiliations

Soon will be listed here.

Abstract

A fundamental feature of auditory perception is the constancy of sound recognition over a large range of intensities. Although this invariance has been described in behavioral studies, the underlying neural mechanism is essentially unknown. Here we show a putative level-invariant representation of sounds by populations of neurons in primary auditory cortex (A1) that may provide a neural basis for the behavioral observations. Previous studies reported that pure-tone frequency tuning of most A1 neurons widens with increasing sound level. In sharp contrast, we found that a large proportion of neurons in A1 of awake marmosets were narrowly and separably tuned to both frequency and sound level. Tuning characteristics and firing rates of the neural population were preserved across all tested sound levels. These response properties lead to a level-invariant representation of sounds over the population of A1 neurons. Such a representation is an important step for robust feature recognition in natural environments.

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References

Shamma S, Fleshman J, Wiser P, Versnel H . Organization of response areas in ferret primary auditory cortex. J Neurophysiol. 1993; 69(2):367-83. DOI: 10.1152/jn.1993.69.2.367. View

Moshitch D, Las L, Ulanovsky N, Bar-Yosef O, Nelken I . Responses of neurons in primary auditory cortex (A1) to pure tones in the halothane-anesthetized cat. J Neurophysiol. 2006; 95(6):3756-69. DOI: 10.1152/jn.00822.2005. View

Phillips D, Orman S . Responses of single neurons in posterior field of cat auditory cortex to tonal stimulation. J Neurophysiol. 1984; 51(1):147-63. DOI: 10.1152/jn.1984.51.1.147. View

Phillips D, Cynader M . Some neural mechanisms in the cat's auditory cortex underlying sensitivity to combined tone and wide-spectrum noise stimuli. Hear Res. 1985; 18(1):87-102. DOI: 10.1016/0378-5955(85)90112-1. View

Spirou G, Young E . Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by bandlimited noise. J Neurophysiol. 1991; 66(5):1750-68. DOI: 10.1152/jn.1991.66.5.1750. View

Kadia S, Wang X . Spectral integration in A1 of awake primates: neurons with single- and multipeaked tuning characteristics. J Neurophysiol. 2003; 89(3):1603-22. DOI: 10.1152/jn.00271.2001. View

Williford T, Maunsell J . Effects of spatial attention on contrast response functions in macaque area V4. J Neurophysiol. 2006; 96(1):40-54. DOI: 10.1152/jn.01207.2005. View

Phillips D, Semple M, Calford M, Kitzes L . Level-dependent representation of stimulus frequency in cat primary auditory cortex. Exp Brain Res. 1994; 102(2):210-26. DOI: 10.1007/BF00227510. View

Ramachandran R, Davis K, May B . Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J Neurophysiol. 1999; 82(1):152-63. DOI: 10.1152/jn.1999.82.1.152. View

10.

HIND J, Goldberg J, GREENWOOD D, Rose J . Some discharge characteristics of single neurons in the inferior colliculus of the cat. II. Timing of the discharges and observations on binaural stimulation. J Neurophysiol. 1963; 26:321-41. DOI: 10.1152/jn.1963.26.2.321. View

11.

Pack C, Berezovskii V, Born R . Dynamic properties of neurons in cortical area MT in alert and anaesthetized macaque monkeys. Nature. 2002; 414(6866):905-8. DOI: 10.1038/414905a. View

12.

Suga N . Classification of inferior collicular neurones of bats in terms of responses to pure tones, FM sounds and noise bursts. J Physiol. 1969; 200(2):555-74. PMC: 1350482. DOI: 10.1113/jphysiol.1969.sp008708. View

13.

Suga N . Philosophy and stimulus design for neuroethology of complex-sound processing. Philos Trans R Soc Lond B Biol Sci. 1992; 336(1278):423-8. DOI: 10.1098/rstb.1992.0078. View

14.

Brugge J, Merzenich M . Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J Neurophysiol. 1973; 36(6):1138-58. DOI: 10.1152/jn.1973.36.6.1138. View

15.

Tan A, Zhang L, Merzenich M, Schreiner C . Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol. 2004; 92(1):630-43. DOI: 10.1152/jn.01020.2003. View

16.

Smith E, Lewicki M . Efficient auditory coding. Nature. 2006; 439(7079):978-82. DOI: 10.1038/nature04485. View

17.

Brincat S, Connor C . Dynamic shape synthesis in posterior inferotemporal cortex. Neuron. 2006; 49(1):17-24. DOI: 10.1016/j.neuron.2005.11.026. View

18.

Polley D, Steinberg E, Merzenich M . Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci. 2006; 26(18):4970-82. PMC: 6674159. DOI: 10.1523/JNEUROSCI.3771-05.2006. View

19.

Cheung S, Bedenbaugh P, Nagarajan S, Schreiner C . Functional organization of squirrel monkey primary auditory cortex: responses to pure tones. J Neurophysiol. 2001; 85(4):1732-49. DOI: 10.1152/jn.2001.85.4.1732. View

20.

Phillips D, Irvine D . Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. J Neurophysiol. 1981; 45(1):48-58. DOI: 10.1152/jn.1981.45.1.48. View