Dissociation of neural mechanisms underlying orientation processing in humans.
Orientation selectivity is a fundamental, emergent property of neurons in early visual cortex, and the discovery of that property has dramatically shaped how we conceptualize visual processing. However, much remains unknown about the neural substrates of this basic building block of perception, and what is known primarily stems from animal physiology studies. To probe the neural concomitants of orientation processing in humans, we employed repetitive transcranial magnetic stimulation (rTMS), which can significantly attenuate neuronal spiking activity, hemodynamic responses, and local field potentials within a focused cortical region. Using rTMS to suppress neural responses evoked by stimuli falling within a local region of the visual field, we were able to dissociate two distinct components of the neural circuitry underlying orientation processing: selectivity and contextual effects. Orientation selectivity gauged by masking was unchanged by rTMS, whereas an otherwise robust orientation repulsion illusion was weakened after rTMS. This dissociation implies that orientation processing in humans relies on distinct mechanisms, only one of which was impacted by rTMS. These results are consistent with models positing that orientation selectivity is governed by patterns of convergence of thalamic afferents onto cortical neurons, with intracortical activity then shaping population responses amongst those cortical neurons.
Ling
Sam
S
Vanderbilt Vision Research Center, Vanderbilt University, Nashville, TN 37204, USA. s.ling@vanderbilt.edu
Pearson
Joel
J
Blake
Randolph
R
D000200:Action Potentials; D006801:Humans; D008954:Models, Biological; D009475:Neurons, Afferent / Q000502:physiology; D009949:Orientation / Q000502:physiology*; D010775:Photic Stimulation; D050781:Transcranial Magnetic Stimulation; D014796:Visual Perception / Q000502:physiology
Science. 2007 Sep 28;317(5846):1918-21
17901333
J Opt Soc Am. 1980 Dec;70(12):1458-71
7463185
Nat Rev Neurosci. 2007 Jul;8(7):522-35
17585305
J Physiol. 1962 Jan;160:106-54
14449617
Proc Biol Sci. 2000 Sep 7;267(1454):1705-10
12233765
Neuron. 2003 Jun 5;38(5):689-99
12797955
Nature. 2000 Jul 13;406(6792):147-50
10910346
Psychol Sci. 2009 Nov;20(11):1348-55
19788529
Science. 1988 Apr 15;240(4850):338-40
3353728
J Neurosci. 1989 Dec;9(12):4287-302
2593002
J Neurophysiol. 1979 Sep;42(5):1264-70
490197
Nat Neurosci. 1999 Aug;2(8):767-71
10412068
Curr Biol. 2005 Dec 6;15(23):2142-8
16332541
Nature. 1996 Mar 21;380(6571):249-52
8637573
J Vis. 2005 Jun 30;5(6):556-70
16097868
J Neurophysiol. 2002 Aug;88(2):888-913
12163540
Exp Brain Res. 1972;15(4):439-40
5079475
Vision Res. 1985;25(10):1459-67
4090280
J Physiol. 1968 Mar;195(1):215-43
4966457
Neuron. 1998 Jun;20(6):1177-89
9655505
Curr Biol. 2004 May 4;14(9):744-51
15120065
Neuron. 2009 Apr 30;62(2):291-303
19409273
Eur J Neurosci. 2004 Apr;19(7):1950-62
15078569
Vision Res. 2009 Jan;49(1):164-72
18977381
Exp Brain Res. 1982;46(3):457-61
7095050
Nat Neurosci. 2005 Feb;8(2):194-201
15665876
Vision Res. 1985;25(10):1469-76
4090281
J Neurosci. 2001 Jun 1;21(11):4002-15
11356887
J Neurosci. 1995 Aug;15(8):5448-65
7643194
Vis Neurosci. 1992 Aug;9(2):181-97
1504027
Curr Opin Neurobiol. 1997 Aug;7(4):514-22
9287203
Vision Res. 2000;40(20):2711-22
10960647
Neuron. 2008 Feb 28;57(4):482-97
18304479
Science. 1994 May 27;264(5163):1333-6
8191289
J Neurosci. 1998 Aug 1;18(15):5908-27
9671678
Vision Res. 2002 Apr;42(9):1165-84
11997055
Annu Rev Neurosci. 2000;23:441-71
10845071