Where orientation tuning arises

Abstract

Introduction: The neural circuitry underlying orientation selectivity, a fundamental question in vision, remains the center of controversy. Some advocate a modified feedforward model, originating in connections from LGN to V1, while others maintain that intracortical activity plays a crucial role in shaping selectivity. To test the role of intracortical activity in shaping orientation selectivity in humans, we employed TMS to attenuate cortical responses to an oriented stimulus and used noise masking to estimate orientation-tuning curves psychophysically. Methods: Prior to each block of experimental trials, we applied TMS pulses at 1 Hz continuously for 2.5 minutes, thereby depressing neural activity at a specific retinotopic site in early visual cortex including V1. In each trial, a filtered noise patch appeared inside or outside the visual region corresponding to the TMS site. A vertically oriented Gabor was embedded within the upper or lower portion of this noise patch, for which observers performed a 2AFC location discrimination task. To obtain psychophysical tuning functions, we used an orientation-bandpass noise masking procedure in which the noise and probe ranged from being identical in orientation, to the noise orientations being orthogonal to the Gabor probe. An adaptive procedure produced estimates of contrast thresholds for the probe embedded within varying orientation bandpass noise, yielding tuning curves for conditions when the stimuli appeared within or outside of the TMS site. Results and Conclusion: Contrast thresholds were elevated for several minutes following TMS (but only at the TMS site), confirming its effectiveness at depressing neural activity at that location. Orientation-tuning bandwidths, however, were unchanged by TMS stimulation. To confirm that TMS disrupts intracortical activity, we found that TMS weakens an illusion known to involve intracortical interactions. These results imply that orientation tuning is governed largely by thalamocortical feedforward signals, with intracortical activity contributing little to the sharpness of orientation tuning.