Physical limits to spatial resolution of optical recording: clarifying the spatial structure of cortical hypercolumns.
Neurons in macaque primary visual cortex are spatially arranged by their global topographic position and in at least three overlapping local modular systems: ocular dominance columns, orientation pinwheels, and cytochrome oxidase (CO) blobs. Individual neurons in the blobs are not tuned to orientation, and populations of neurons in the pinwheel center regions show weak orientation tuning, suggesting a close relation between pinwheel centers and CO blobs. However, this hypothesis has been challenged by a series of optical recording experiments. In this report, we show that the statistical error associated with photon scatter and absorption in brain tissue combined with the blurring introduced by the optics of the imaging system has typically been in the range of 250 microm. These physical limitations cause a systematic error in the location of pinwheel centers because of the vectorial nature of these patterns, such that the apparent location of a pinwheel center measured by optical recording is never (on average) in the correct in vivo location. The systematic positional offset is approximately 116 microm, which is large enough to account for the claimed misalignment of CO blobs and pinwheel centers. Thus, optical recording, as it has been used to date, has insufficient spatial resolution to accurately locate pinwheel centers. The earlier hypothesis that CO blobs and pinwheel centers are coterminous remains the only hypothesis currently supported by reliable observation.
Polimeni
Jonathan R
JR
Department of Electrical and Computer Engineering, Boston University, Boston, MA 02215, USA.
Granquist-Fraser
Domhnull
D
Wood
Richard J
RJ
Schwartz
Eric L
EL
D000818:Animals; D003198:Computer Simulation; D003576:Electron Transport Complex IV / Q000502:physiology; D008251:Macaca; D009010:Monte Carlo Method; D009474:Neurons / Q000502:physiology*; D014793:Visual Cortex / Q000502:physiology*
D003576:Electron Transport Complex IV
Neuroimage. 2003 Nov;20(3):1857-64
14642495
Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4057-60
10097162
J Neurosci. 1984 Jan;4(1):309-56
6198495
J Neurosci. 1983 Nov;3(11):2251-62
6631479
IEEE Trans Image Process. 1997;6(12):1646-58
18285235
J Neurosci. 1993 Oct;13(10):4157-80
8410182
J Neurosci. 1992 Aug;12(8):3139-61
1322982
J Physiol. 1962 Jan;160:106-54
14449617
Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11905-9
1465416
J Neurophysiol. 1957 Jul;20(4):408-34
13439410
Nature. 1981 Aug 20;292(5825):762-4
6267472
Appl Opt. 2003 Jun 1;42(16):3321-9
12790485
Nature. 1986 Nov 27-Dec 3;324(6095):361-4
3785405
J Comp Neurol. 1974 Dec 1;158(3):295-305
4436457
Nat Rev Neurosci. 2004 Nov;5(11):874-85
15496865
J Neurosci. 1996 Nov 15;16(22):7228-39
8929431
IEEE Trans Pattern Anal Mach Intell. 2007 May;29(5):807-23
17356201
Biol Cybern. 1990;62(5):381-91
2110005
Nature. 1986 Jun 5-11;321(6070):579-85
3713842
Science. 1997 Jun 6;276(5318):1551-5
9171056
Philos Trans R Soc Lond B Biol Sci. 1984 Jan 17;304(1119):255-72
6142485
J Neurosci Methods. 1991 Feb;36(2-3):127-37
1905769
J Neurosci. 2004 Jul 14;24(28):6237-47
15254078
J Neurosci. 2001 Oct 15;21(20):8286-301
11588200
Neuron. 1997 Mar;18(3):351-7
9115730
Science. 1990 Jul 27;249(4967):417-20
2165630
Proc R Soc Lond B Biol Sci. 1977 Jul 28;198(1130):1-59
20635
Biol Cybern. 1979 Aug 1;33(3):179-86
497262