Elsevier

Neuropsychologia

Volume 37, Issue 2, 1 November 1998, Pages 137-145
Neuropsychologia

Two periods of processing in the (circum)striate visual cortex as revealed by transcranial magnetic stimulation

https://doi.org/10.1016/S0028-3932(98)00088-8Get rights and content

Abstract

To determine the timing of visual processing in the (circum)striate visual cortex, we examined the effect of single pulse transcranial magnetic stimulation over the occipital pole of healthy subjects who were engaged in a forced-choice visual letter identification task. Single letters, subtending a visual angle of 0.35°, were foveally presented for 10 ms and were immediately followed by a mask. We investigated 30 different delays (d), defined as the time between the onset of the visual stimulus and the onset of the magnetic stimulus, from d = −100 ms to d = +190 ms, and 4 different midsagittal coil positions (x), defined as the distance between the lower edge of the coil and the upper edge of the inion, from x = 1 cm to x = 7 cm. Three out of four subjects showed three distinct delay intervals (dips) at which application of TMS resulted in an impairment of the task. The first dip was centred around d = −50 ms and occurred independently of the coil position; the second dip was centred around d = 0 ms and was elicitable only with the two lowest coil positions; the third dip was centred around d = 100 ms and was also elicitable only with the lower coil positions. In the fourth subject, only the first and the third dip were found. We conclude that there are two distinct periods when the activity in the (circum)striate visual cortex is necessary for the identification of visually presented letters.

Introduction

With the technique of transcranial magnetic stimulation (TMS), it is possible to disrupt the activity in the underlying neural tissue. When the application of TMS over a particular cortical area suppresses the performance of some particular task or function, we can infer that that area is necessary for that task or function (with a spatial resolution of the order of 10 mm). By then looking at the precise timing at which TMS causes suppression, we can also infer when the activity of that area is necessary for that task or function (with a temporal resolution of the order of 1 to 10 ms). Amassian et al. [1]were the first to demonstrate suppression of visual perception with TMS: subjects were unable to identify visually presented letters whenever a TMS pulse was given over the occipital pole between 80 ms and 100 ms after the onset of the presentation of the letter. Although Beckers and Homberg [3]and Beckers and Zeki [4]reported suppression of visual perception at much earlier times in a motion direction discrimination task with TMS over V5, they 3, 4, together with all other investigators 2, 9, 10, 13, 15reported suppression with TMS over the occipital pole only at about the same (later) times as those first reported by Amassian et al. [1]. The aim of our experiments was to achieve suppression of visual perception with TMS over the occipital pole at much earlier times, corroborating cellular recording experiments in primates 6, 7, 11, 14, 16, 20and in humans [21]that show striate cortical activity starting as early as 20 ms [14], 27 ms [16], 30 ms [7], 31 ms [21], 36 ms [11], 41 ms [6], and 20–40 ms [20]after the onset of the visual stimulus. We hoped to achieve this by presenting subjects with small, individual letters confined to the foveal region, at high contrast, for a short time, and with immediate postmasking, which collectively should ensure that the cortical processing has an early onset, a short duration, and a high sensitivity to TMS.

Section snippets

Methods

The main goal of Experiment 1 was to investigate the times at which TMS could suppress the visual identification of a letter when it was presented with very high spatial and temporal limitations. The critical independent variable was the delay (d ), defined as the time between the onset of the visual stimulus and the onset of the magnetic stimulus, ranging from d = −100 ms to d = 190 ms, in steps of 10 ms. In defining the delay, we took into account the 5 ms that it takes the electron beam, at a

Methods

The main goal of Experiment 2 was to show whether (any part of) the wide early dip present in three out of four subjects (s = 2, s = 3, s = 4) was indeed attributable to disruption of activity in the visual cortex. The methods were the same as in Experiment 1 with the following exceptions. First, Experiment 2 had two critical independent variables: the delay (d), defined as the time between the onset of the visual stimulus and the onset of the magnetic stimulus (d = −60 ms, d = −50 ms, d = −10

General Discussion

The results of Experiment 1 corroborated the results of previous investigators 1, 2, 3, 4, 9, 10, 13, 15in that they showed a late dip with the TMS coil placed over the occipital pole. This late dip invariably started at delay d = 60 ms, and descended steeply towards delays d = 90 ms and d = 100 ms, where letter identification was abolished. More importantly, in three out of four subjects, we also found a wide early dip, that invariably ended at delay d = 50 ms, but whose start showed a

Acknowledgements

Erik Corthout was supported by a D. Collen Research Foundation Fellowship. Bob Uttl was supported by the Henry Jackson Foundation. Ulf Ziemann was supported by grant Zi 542/1-1 from the Deutsche Forschungsgemeinschaft.

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