Two phases of V1 activity for visual recognition of natural images

Abstract

Present theories of visual recognition emphasize the role of interactive processing across populations of neurons within a given network, but the nature of these interactions remains unresolved. In particular, data describing the sufficiency of feedforward algorithms for conscious vision and studies revealing the functional relevance of feedback connections to the striate cortex seem to offer contradictory accounts of visual information processing. TMS is a good method to experimentally address this issue, given its excellent temporal resolution and its capacity to establish causal relations between brain function and behavior. We studied 20 healthy volunteers in a visual recognition task. Subjects were briefly presented with images of animals (birds or mammals) in natural scenes and were asked to indicate the animal category. MRI-guided stereotaxic single TMS pulses were used to transiently disrupt striate cortex function at different times after image onset (SOA). Visual recognition was significantly impaired when TMS was applied over the occipital pole at SOAs of 100 and 220 msec. The first interval has consistently been described in previous TMS studies and is explained as the interruption of the feedforward volley of activity. Given the late latency and discrete nature of the second peak, we hypothesize that it represents the disruption of a feedback projection to V1, probably from other areas in the visual network. These results provide causal evidence for the necessity of recurrent interactive processing, through feedforward and feedback connections, in visual recognition of natural complex images.

Figure 1

Experimental design. Images were flashed for one refreshment rate (14 msec) and subjects were asked to categorize the images with a button click. Following image presentation, a single pulse of TMS was applied at any one of 15 possible SOAs (from 20 to 300 msec). The next image appeared 3000 msec after the TMS pulse.

Figure 2

Changes in visual categorization induced by TMS. (A) Contrasts of the results obtained with 10 subjects in Experiment 1 (red) and 10 different subjects in Experiment 2 (blue). Experiment 1 involved extensive learning of the visual stimuli and practice in the task. TMS was unable to induce any significant changes in performance. In Experiment 2, subjects had never seen the images or practiced the task. These results reflect the changes in performance induced by single pulses of TMS at different SOAs for novel images. (B) The results of Experiment 2 in detail. The SEM is highlighted in dotted lines, and the significant SOAs are marked in orange. TMS was capable of significantly impairing recognition at two different time points: 100 and 220 msec.