Location coding by opponent neural populations in the auditory cortex.
Although the auditory cortex plays a necessary role in sound localization, physiological investigations in the cortex reveal inhomogeneous sampling of auditory space that is difficult to reconcile with localization behavior under the assumption of local spatial coding. Most neurons respond maximally to sounds located far to the left or right side, with few neurons tuned to the frontal midline. Paradoxically, psychophysical studies show optimal spatial acuity across the frontal midline. In this paper, we revisit the problem of inhomogeneous spatial sampling in three fields of cat auditory cortex. In each field, we confirm that neural responses tend to be greatest for lateral positions, but show the greatest modulation for near-midline source locations. Moreover, identification of source locations based on cortical responses shows sharp discrimination of left from right but relatively inaccurate discrimination of locations within each half of space. Motivated by these findings, we explore an opponent-process theory in which sound-source locations are represented by differences in the activity of two broadly tuned channels formed by contra- and ipsilaterally preferring neurons. Finally, we demonstrate a simple model, based on spike-count differences across cortical populations, that provides bias-free, level-invariant localization-and thus also a solution to the "binding problem" of associating spatial information with other nonspatial attributes of sounds.
Stecker
G Christopher
GC
Kresge Hearing Research Institute, University of Michigan, Ann Arbor, Michigan, USA. cstecker@ebire.org <cstecker@ebire.org>
Harrington
Ian A
IA
Middlebrooks
John C
JC
D000161:Acoustic Stimulation; D000818:Animals; D001303:Auditory Cortex / Q000502:physiology*; D001931:Brain Mapping / Q000379:methods; D002415:Cats; D023421:Models, Animal; D008959:Models, Neurological; D009474:Neurons / Q000502:physiology*; D013017:Sound Localization / Q000502:physiology*
Vision Res. 1993 May;33(8):1053-65
8506645
J Acoust Soc Am. 1975 Jan;57(1):181-7
1110279
Hear Res. 1981 Jul;4(3-4):299-307
7263517
J Neurosci. 1984 Jul;4(7):1781-6
6737040
J Neurophysiol. 2004 Sep;92(3):1625-43
15331649
Annu Rev Psychol. 1985;36:245-74
3883890
J Neurosci. 2003 Jan 15;23(2):716-24
12533632
Neuron. 1999 Sep;24(1):87-93, 111-25
10677029
Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):14050-4
11707595
J Neurophysiol. 1990 Sep;64(3):872-87
2230931
J Neurophysiol. 2004 Jan;91(1):118-35
14523080
J Neurophysiol. 1987 Jun;57(6):1746-66
3598629
Brain Res. 1977 Dec 16;138(2):241-57
589474
J Neurophysiol. 2002 Apr;87(4):1749-62
11929896
J Acoust Soc Am. 1998 Apr;103(4):2064-8
9566328
J Neurosci. 1984 Oct;4(10):2621-34
6491727
J Neurosci. 2004 Aug 11;24(32):7110-7
15306644
Hear Res. 2005 Jan;199(1-2):124-34
15574307
J Neurophysiol. 1985 Aug;54(2):185-211
4031984
J Acoust Soc Am. 1999 Oct;106(4 Pt 1):1948-55
10530019
J Comp Neurol. 1980 Aug 1;192(3):455-72
7419739
Acta Otolaryngol Suppl. 1997;532:22-7
9442840
J Neurosci. 1998 Mar 15;18(6):2147-60
9482800
J Neurophysiol. 2005 Mar;93(3):1223-34
15483065
J Comp Physiol Psychol. 1948 Feb;41(1):35-9
18904764
Hear Res. 1983 May;10(2):203-15
6863155
Nature. 2004 Aug 5;430(7000):682-6
15295602
Behav Brain Res. 1983 May;8(2):211-6
6860463
Brain Res. 1980 Jan 6;181(1):31-48
7350963
J Neurophysiol. 1998 Aug;80(2):863-81
9705474
Biol Cybern. 2003 Nov;89(5):341-9
14669014
J Neurosci. 1981 Jan;1(1):107-20
7346555
J Acoust Soc Am. 1996 Aug;100(2 Pt 1):1059-69
8759959
Neuron. 1999 Sep;24(1):95-104, 111-25
10677030
J Neurophysiol. 1982 Jun;47(6):987-1016
7108581
Exp Neurol. 1972 Jun;35(3):431-49
5035153
Nature. 2002 May 30;417(6888):543-7
12037566
Science. 1978 May 19;200(4343):795-7
644324
Science. 1994 May 6;264(5160):842-4
8171339
J Neurophysiol. 1990 Sep;64(3):915-31
2230934
Hear Res. 1988 Nov;36(2-3):221-32
3209494
J Acoust Soc Am. 2004 Apr;115(4):1705-13
15101649
Exp Brain Res. 1991;86(3):483-505
1722171
J Neurophysiol. 1987 Apr;57(4):1185-200
3585459
Nat Neurosci. 2001 Apr;4(4):396-401
11276230
J Neurosci. 1982 Sep;2(9):1177-94
7119872
J Neurophysiol. 2003 Jun;89(6):2889-903
12611946
Hear Res. 1985 Mar;17(3):267-80
4019332
J Neurosci. 1996 Jul 15;16(14):4420-37
8699253
Biol Cybern. 2003 Nov;89(5):378-87
14669018