Details

Autor(en) / Beteiligte

• Butler, R.
• Mierzwinski, G.W.
• Bernier, P.M.
• Descoteaux, M.
• Gilbert, G.
• Whittingstall, K.

Titel

Neurophysiological basis of contrast dependent BOLD orientation tuning

Ist Teil von

• NeuroImage (Orlando, Fla.), 2020-02, Vol.206, p.116323-116323, Article 116323

Ort / Verlag

United States: Elsevier Inc

Erscheinungsjahr

2020

Link zum Volltext

Quelle

MEDLINE

Beschreibungen/Notizen

• Recent work in early visual cortex of humans has shown that the BOLD signal exhibits contrast dependent orientation tuning, with an inverse oblique effect (oblique > cardinal) at high contrast and a horizontal effect (vertical > horizontal) at low contrast. This finding is at odds with decades of neurophysiological research demonstrating contrast invariant orientation tuning in primate visual cortex, yet the source of this discrepancy is unclear. We hypothesized that contrast dependent BOLD orientation tuning may arise due to contrast dependent influences of feedforward (FF) and feedback (FB) synaptic activity, indexed through gamma and alpha rhythms, respectively. To quantify this, we acquired EEG and BOLD in healthy humans to generate and compare orientation tuning curves across all neural frequency bands with BOLD. As expected, BOLD orientation selectivity in V1 was contrast dependent, preferring oblique orientations at high contrast and vertical at low contrast. On the other hand, EEG orientation tuning was contrast invariant, though frequency-specific, with an inverse-oblique effect in the gamma band (FF) and a horizontal effect in the alpha band (FB). Therefore, high-contrast BOLD orientation tuning closely matched FF activity, while at low contrast, BOLD best resembled FB orientation tuning. These results suggest that contrast dependent BOLD orientation tuning arises due to the reduced contribution of FF input to overall neurophysiological activity at low contrast, shifting BOLD orientation tuning towards the orientation preferences of FB at low contrast. •BOLD orientation tuning depends on contrast of grating stimulus.•Inverse-oblique effect in EEG gamma band orientation tuning curve.•Horizontal effect in EEG alpha band orientation tuning curve.•BOLD orientation tuning follows gamma at high contrast, alpha at low contrast.•BOLD measures pooled feedforward/feedback influences. Orientation selectivity is a fundamental property of primary visual cortex (V1) and decades of animal research has shown that orientation preference is contrast invariant. However, fMRI studies using BOLD in humans have revealed that hemodynamic signals can switch orientation preference depending on contrast, yet the mechanism behind this is unclear. Here, we used EEG to resolve this paradox, showing that contrast dependent BOLD orientation tuning arises due to the separate orientation tuning preferences of feedforward (FF) and feedback (FB) synaptic activity, measured through gamma and alpha rhythms respectively. This demonstrates that hemodynamic neuroimaging signals such as BOLD can change their stimulus tuning preferences in ways not expected based on results from conventional neurophysiology experiments and are likely reflecting the totality of synaptic activity arising from both FF and FB influences, which are pooled in the BOLD signal of conventional neuroimaging experiments.