Contrast invariance of orientation tuning in cat primary visual cortex neurons depends on stimulus size

Key points

• The process of orientation tuning is an important and well‐characterized feature of neurons in primary visual cortex.
• The combination of ascending and descending circuits involved is not only relevant to understanding visual processing but the function of neocortex in general.
• The classic feed‐forward model of orientation tuning predicts a broadening effect due to increasing contrast; yet, experimental results consistently report contrast invariance.
• We show here that contrast invariance actually depends on stimulus size such that large stimuli extending beyond the neuron''s receptive field engage circuits that promote invariance, whereas optimally sized, smaller stimuli result in contrast variance that is more in line with the classical orientation tuning model.
• These results illustrate the importance of optimizing stimulus parameters to best reflect the sensory pathways under study and provide new clues about different circuits that may be involved in variant and invariant response properties.

Abstract

Selective response to stimulus orientation is a key feature of neurons in primary visual cortex, yet the underlying mechanisms generating orientation tuning are not fully understood. The combination of feed‐forward and cortical mechanisms involved is not only relevant to understanding visual processing but the function of neocortex in general. The classic feed‐forward model predicts that orientation tuning should broaden considerably with increasing contrast; however, experimental results consistently report contrast invariance. We show here, in primary visual cortex of anaesthetized cats under neuromuscular blockade, that contrast invariance occurs when visual stimuli are large enough to include the extraclassical surround (ECS), which is likely to involve circuits of suppression that may not be entirely feed‐forward in origin. On the other hand, when stimulus size is optimized to the classical receptive field of each neuron, the population average shows a statistically significant 40% increase in tuning width at high contrast, demonstrating that contrast variance of orientation tuning can occur. Conversely, our results also suggest that the phenomenon of contrast invariance relies in part on the presence of the ECS. Moreover, these results illustrate the importance of optimizing stimulus parameters to best reflect the neural pathways under study.

Abbreviations

CRF

classical receptive field

CV

circular variance

ECS

extraclassical receptive field

HWHH

half‐width at half‐height

LGN

lateral geniculate nucleus

V1

primary visual cortex