Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus detection: implications for multisensory interactions

Abstract

Multisensory interactions occur early in time and in low-level cortical areas, including primary cortices. To test current models of early auditory-visual (AV) convergence in unisensory visual brain areas, we studied the effect of transcranial magnetic stimulation (TMS) of visual cortex on behavioral responses to unisensory (auditory or visual) or multisensory (simultaneous auditory-visual) stimulus presentation. Single-pulse TMS was applied over the occipital pole at short delays (30-150 ms) after external stimulus onset. Relative to TMS over a control site, reactions times (RTs) to unisensory visual stimuli were prolonged by TMS at 60-75 ms poststimulus onset (visual suppression effect), confirming stimulation of functional visual cortex. Conversely, RTs to unisensory auditory stimuli were significantly shortened when visual cortex was stimulated by TMS at the same delays (beneficial interaction effect of auditory stimulation and occipital TMS). No TMS-effect on RTs was observed for AV stimulation. The beneficial interaction effect of combined unisensory auditory and TMS-induced visual cortex stimulation matched and was correlated with the RT-facilitation after external multisensory AV stimulation without TMS, suggestive of multisensory interactions between the stimulus-evoked auditory and TMS-induced visual cortex activities. A follow-up experiment showed that auditory input enhances excitability within visual cortex itself (using phosphene-induction via TMS as a measure) over a similarly early time-window (75-120 ms). The collective data support a mechanism of early auditory-visual interactions that is mediated by auditory-driven sensitivity changes in visual neurons that coincide in time with the initial volleys of visual input.

Figure 1.

A, Mean RTs (SEM indicated) to external stimuli at baseline (no TMS) as a function of stimulus-type. B, Group averaged cumulative probability distribution for each stimulus condition and Miller's (1982) model predictions. C, Reaction times to multisensory stimuli exceeded prediction of probability summation over the fastest part of the distribution (indicated by positive values). *p < 0.05.

Figure 2.

RTs (SEM indicated) to external stimuli are represented at baseline (BSL, no TMS) and for each TMS delay from stimulus onset (30–150 ms) as a function of stimulus type (A, V, AV). The curves represent changes in RTs caused by occipital TMS (visual cortex stimulation) relative to control (vertex) stimulation (ΔRT = RT_{occipital TMS} minus RT_{vertex TMS}). An RT benefit for external auditory stimuli (A) when combined with stimulation of visual cortex at TMS-delays of 60–75 ms was observed (gray curve, negative deflection). This coincided in time with a RT cost to external visual stimuli attributable to TMS at the same site (visual suppression, black curve, positive values). The shaded area represents the time window of coincident effects. **p < 0.01; ***p < 0.001; ****p < 0.0001.

Figure 3.

Scatterplot of the correlation between RT facilitations in this study. The x-axis plots the RT facilitation after multisensory stimuli in the absence of TMS (AV minus A). The y-axis plots the RT facilitation after occipital TMS in combination with auditory stimulation (A-occipital TMS minus A-vertex TMS).

Figure 4.

Percentage of perceived phosphenes caused by occipital TMS as a function of TMS-pulse delay from the brief auditory stimulus. TMS was applied below phosphene threshold (85% PT), latter defined at baseline (BSL; i.e., in the absence of any auditory stimulus). The shaded area represents the window of significantly increased visual cortex excitability by auditory input (i.e., phosphene perception > BSL; *p < 0.05; **p < 0.01).