Laminar differences in responses to naturalistic texture in macaque V1 and V2

Abstract

Most single units recorded from macaque V2 respond with higher firing rates to synthetic texture images containing "naturalistic" higher-order statistics than to spectrally matched "noise" images lacking these statistics. In contrast, few single units in V1 show this property. We explored how the strength and dynamics of response vary across the different layers of visual cortex by recording multiunit and gamma band activity evoked by brief presentations of naturalistic and noise images in V1 and V2 of anesthetized macaque monkeys. As previously reported, recordings in V2 showed consistently stronger responses to naturalistic texture than to spectrally matched noise. In contrast to single unit recordings, V1 multiunit activity showed some preference for images with naturalistic statistics, and in gamma band activity this preference was comparable across V1 and V2. Sensitivity to naturalistic image structure was strongest in the supragranular and infragranular layers of V1, but weak in granular layers, suggesting that it might reflect feedback from V2. Response timing was consistent with this idea. Visual responses appeared first in V1, followed by V2. Sensitivity to naturalistic texture emerged first in V2, followed by the supragranular and infragranular layers of V1, and finally in the granular layers of V1. Our results demonstrate laminar differences in the encoding of higher-order statistics of natural texture, and suggest that this sensitivity first arises in V2 and is fed back to modulate activity in V1. Significance StatementThe circuit mechanisms responsible for visual representations of intermediate complexity are largely unknown. We used a well-validated set of synthetic texture stimuli to probe the temporal and laminar profile of sensitivity to the higher-order statistical structure of natural images. We found that this sensitivity emerges first and most strongly in V2 but soon after in V1. However, sensitivity in V1 is higher in the laminae (extragranular) and recording modalities (local field potential) most likely affected by V2 connections, suggesting a feedback origin. Our results show how sensitivity to naturalistic image structure emerges across time and circuitry in the early visual cortex.

Rapid Selectivity to Natural Images Across Layers of Primate V1

“…First, we measured the entire neuronal response (40 - 200 ms from image onset) and calculated a modulation index to quantify response differences between different image types (Methods). Consistent with previous studies 11,14 , we found no significant difference between the magnitude of responses to NTIs and to SMNIs (, p = 0.67, paired t-test). However, the neuronal responses to natural images were consistently larger than those to NTIs (, p < 10 −31 , t-test) and to SMNIs (, p < 10 −42 , paired t-test).…”

“…Our results integrate two lines of work on natural image representation in V1 in the same experiments. On the one hand, consistent with previous studies on natural texture images 14,17,18 , our results show that single V1 neurons does not show significant selectivity to naturalistic textures. Specifically, V1 neurons do not show response differences between naturalistic textures and spectrum-matched noise images even with a large population of simultaneously recorded V1 neurons.…”

“…To further explore the possible origins of the preference for natural images, we next examined the spatiotemporal pattern of sensitivity to natural images across different cortical layers. We considered that if the sensitivity to naturalness in V1 originates from feedback from later visual cortical stages, e.g., V2, then we should observe stronger and earlier developing sensitivity within supragranular and infragranular layers, with weaker and slower developing sensitivity within granular layer 4C 14,24,25 . Using the simultaneously recorded activity, we compared the sensitivity to natural images for neurons distributed across laminar compartments (Fig.…”

“…This latter approach was first used to study neuronal responses at the late stages of visual processing in macaque cortex where it was found that single neurons in V4 and IT show higher sensitivity to natural images than naturalistic textures 12,13,16 . Later work in V1 and V2 found that single V1 neurons are insensitive to the pair-wise correlation structure present in NTIs, and that sensitivity to this mid-level structure first emerges in V2 11,14,17 . A study in human visual cortex compared BOLD responses to SMNIs, NTIs, and natural images and found an orderly progression where selectivity to natural images emerged first in areas anterior to V3, such as V4, while selectivity to (which was not certified by peer review) is the author/funder.…”

“…A fruitful approach to studying natural images processing has been to compare responses to synthetic images matched on various summary statistics to those of natural images [11][12][13][14] . One of these synthetic image types comprises images that match the power spectrum of corresponding natural images, spectrum-matched noise images (SMNIs).…”