Effects of attention on visual processing between cortical layers and cortical areas V1 and V4

Visual attention improves sensory processing, as well as perceptual readout and behavior. Over the last decades, many proposals have been put forth to explain how attention affects visual neural processing. These include the modulation of neural firing rates and synchrony, neural tuning properties, and rhythmic, subthreshold activity. Despite the wealth of knowledge provided by previous studies, the way attention shapes interactions between cortical layers within and between visual sensory areas is only just emerging. To investigate this, we studied neural signals from macaque V1 and V4 visual areas, while monkeys performed a covert, feature-based spatial attention task. The data were simultaneously recorded from laminar electrodes disposed normal to cortical surface in both areas (16 contacts, 150 μm inter-contact spacing). Stimuli presentation was based on the overlap of the receptive fields (RFs) of V1 and V4. Channel depths alignment was referenced to laminar layer IV, based on spatial current source density and temporal latency analyses. Our analyses mainly focused on the study of Local Field Potential (LFP) signals, for which we applied local (bipolar) re-referencing offline. We investigated the effects of attention on LFP spectral power and laminar interactions between LFP signals at different depths, both at the local level within V1 and V4, and at the inter-areal level across V1 and V4. Inspired by current progress from literature, we were interested in the characterization of frequency-specific laminar interactions, which we investigated both in terms of rhythmic synchronization by computing spectral coherence, and in terms of directed causal influence, by computing Granger causalities (GCs). The spectral power of LFPs in different frequency bands showed relatively small differences along cortical depths both in V1 and in V4. However, we found attentional effects on LFP spectral power consistent with previous literature. For V1 LFPs, attention to stimuli in RF location mainly resulted in a shift of the low-gamma (∼30-50 Hz) spectral power peak towards (∼3-4 Hz) higher frequencies and increases in power for frequency bands above low-gamma peak frequencies, as well as decreases in power below these frequencies. For V4 LFPs, attention towards stimuli in RF locations caused a decrease in power for frequencies < 20 Hz and a broad band increase for frequencies > 20 Hz. Attention affected spectral coherence within V1 and within V4 layers in similar way as the spectral power modulation described above. Spectral coherence between V1 and V4 channel pairs was increased by attention mainly in the beta band (∼ 15-30 Hz) and the low-gamma range (∼ 30-50 Hz). Attention affected GC interactions in a layer and frequency dependent manner in complex ways, not always compliant with predictions made by the canonical models of laminar feed-forward and feed-back interactions. Within V1, attention increased feed-forward efficacy across almost all low-frequency bands (∼ 2-50 Hz). Within V4, attention mostly increased GCs in the low and high gamma frequency in a 'downwards' direction within the column, i.e. from supragranular to granular and to infragranular layers. Increases were also evident in an ‘upwards’ direction from granular to supragranular layers. For inter-areal GCs, the dominant changes were an increase in the gamma frequency range from V1 granular and infragranular layers to V4 supragranular and granular layers, as well as an increase from V4 supragranular layers to all V1 layers.