Visually Driven Activation in Macaque Areas V2 and V3 without Input from the Primary Visual Cortex

Michael C Schmid,Nikos K Logothetis,Stelios M Smirnakis,Theofanis Panagiotaropoulos,Mark A Augath

doi:10.1371/journal.pone.0005527

Michael C Schmid, Nikos K Logothetis + Show 3 more

Open Access

PDF Available

https://doi.org/10.1371/journal.pone.0005527

Copy DOI

Export

Save

Cite

Abstract
Highlights/Summary
Full-Text PDF
Similar Papers

Abstract

Listen

Creating focal lesions in primary visual cortex (V1) provides an opportunity to study the role of extra-geniculo-striate pathways for activating extrastriate visual cortex. Previous studies have shown that more than 95% of neurons in macaque area V2 and V3 stop firing after reversibly cooling V1 [1], [2], [3]. However, no studies on long term recovery in areas V2, V3 following permanent V1 lesions have been reported in the macaque. Here we use macaque fMRI to study area V2, V3 activity patterns from 1 to 22 months after lesioning area V1. We find that visually driven BOLD responses persist inside the V1-lesion projection zones (LPZ) of areas V2 and V3, but are reduced in strength by ∼70%, on average, compared to pre-lesion levels. Monitoring the LPZ activity over time starting one month following the V1 lesion did not reveal systematic changes in BOLD signal amplitude. Surprisingly, the retinotopic organization inside the LPZ of areas V2, V3 remained similar to that of the non-lesioned hemisphere, suggesting that LPZ activation in V2, V3 is not the result of input arising from nearby (non-lesioned) V1 cortex. Electrophysiology recordings of multi-unit activity corroborated the BOLD observations: visually driven multi-unit responses could be elicited inside the V2 LPZ, even when the visual stimulus was entirely contained within the scotoma induced by the V1 lesion. Restricting the stimulus to the intact visual hemi-field produced no significant BOLD modulation inside the V2, V3 LPZs. We conclude that the observed activity patterns are largely mediated by parallel, V1-bypassing, subcortical pathways that can activate areas V2 and V3 in the absence of V1 input. Such pathways may contribute to the behavioral phenomenon of blindsight.

Highlights

The flow of visual information from the retina to the higher cognitive and motor areas contains a series of transformation steps involving a number of subcortical and cortical brain areas
Histological (Figure 1B) and radiological (Figure 1C) examination effectively ruled out the possibility that visually driven responses in areas V2, V3 might be due to surviving gray matter tissue within the area of the V1 lesion itself
To examine the influence of the V1 lesion on V2 and V3 activity, we identified retinotopically the V1-lesion projection zones (LPZ) in these areas

Summary

Introduction

The flow of visual information from the retina to the higher cognitive and motor areas contains a series of transformation steps involving a number of subcortical and cortical brain areas. The primary visual cortex (V1) is considered to be the major entry point for cortical visual processing and activity in subsequent ‘‘higher’’ visual areas is generally interpreted as arising primarily from a transformation of V1 input. This model has been highly successful for studying how visual information is transformed across areas, it is clear that it provides only a partial description of the actual information flow. To date the role that these pathways play in visual processing is at best poorly understood

Methods

Results

Conclusion