A vast amount of information about the external world continuously flows into the brain, whereas its capacity to process such information is limited. Attention enables the brain to allocate its resources of information processing to selected sensory inputs for reducing its computational load, and effects of attention have been extensively studied in visual information processing. However, how the microcircuit of the visual cortex processes attentional information from higher areas remains largely unknown. Here, we explore the complex interactions between visual inputs and an attentional signal in a computational model of the visual cortical microcircuit. Our model not only successfully accounts for previous experimental observations of attentional effects on visual neuronal responses, but also predicts contrasting differences in the attentional effects of top-down signals between cortical layers: attention to a preferred stimulus of a column enhances neuronal responses of layers 2/3 and 5, the output stations of cortical microcircuits, whereas attention suppresses neuronal responses of layer 4, the input station of cortical microcircuits. We demonstrate that the specific modulation pattern of layer-4 activity, which emerges from inter-laminar synaptic connections, is crucial for a rapid shift of attention to a currently unattended stimulus. Our results suggest that top-down signals act differently on different layers of the cortical microcircuit.

Various subtypes of inhibitory interneurons contact one another to organize cortical networks. Most cortical inhibitory interneurons express 1 of 3 genes: parvalbumin (PV), somatostatin (SOM), or vasoactive intestinal polypeptide (VIP). This diversity of inhibition allows the flexible regulation of neuronal responses within and between cortical areas. However, the exact roles of these interneuron subtypes and of excitatory pyramidal (Pyr) neurons in regulating neuronal network activity and establishing perception (via interactions between feedforward sensory and feedback attentional signals) remain largely unknown. To explore the regulatory roles of distinct neuronal types in cortical computation, we developed a computational microcircuit model with biologically plausible visual cortex layers 2/3 that combined Pyr neurons and the 3 inhibitory interneuron subtypes to generate network activity. In simulations with our model, inhibitory signals from PV and SOM neurons preferentially induced neuronal firing at gamma (30–80 Hz) and beta (20–30 Hz) frequencies, respectively, in agreement with observed physiological results. Furthermore, our model indicated that rapid inhibition from VIP to SOM subtypes underlies marked attentional modulation for low-gamma frequency (30–50 Hz) in Pyr neuron responses. Our results suggest the distinct but cooperative roles of inhibitory interneuron subtypes in the establishment of visual perception.

Analysis and understanding of trained deep neural networks (DNNs) can deepen our understanding of the visual mechanisms involved in primate visual perception. However, due to the limited availability of neural activity data recorded from various cortical areas, the correspondence between the characteristics of artificial and biological neural responses for visually recognizing objects remains unclear at the layer level of DNNs. In the current study, we investigated the relationships between the artificial representations in each layer of a trained AlexNet model (based on a DNN) for object classification and the neural representations in various levels of visual cortices such as the primary visual (V1), intermediate visual (V4), and inferior temporal cortices. Furthermore, we analyzed the profiles of the artificial representations at a single channel level for each layer of the AlexNet model. We found that the artificial representations in the lower-level layers of the trained AlexNet model were strongly correlated with the neural representation in V1, whereas the responses of model neurons in layers at the intermediate and higher-intermediate levels of the trained object classification model exhibited characteristics similar to those of neural activity in V4 neurons. These results suggest that the trained AlexNet model may gradually establish artificial representations for object classification through the hierarchy of its network, in a similar manner to the neural mechanisms by which afferent transmission beginning in the low-level features gradually establishes object recognition as signals progress through the hierarchy of the ventral visual pathway.

The activity of a border ownership selective (BOS) neuron indicates where a foreground object is located relative to its (classical) receptive field (RF). A population of BOS neurons thus provides an important component of perceptual grouping, the organization of the visual scene into objects. In previous theoretical work, it has been suggested that this grouping mechanism is implemented by a population of dedicated grouping (“G”) cells that integrate the activity of the distributed feature cells representing an object and, by feedback, modulate the same cells, thus making them border ownership selective. The feedback modulation by G cells is thought to also provide the mechanism for object-based attention. A recent modeling study showed that modulatory common feedback, implemented by synapses with N-methyl-D-aspartate (NMDA)-type glutamate receptors, accounts for the experimentally observed synchrony in spike trains of BOS neurons and the shape of cross-correlations between them, including its dependence on the attentional state. However, that study was limited to pairs of BOS neurons with consistent border ownership preferences, defined as two neurons tuned to respond to the same visual object, in which attention decreases synchrony. But attention has also been shown to increase synchrony in neurons with inconsistent border ownership selectivity. Here we extend the computational model from the previous study to fully understand these effects of attention. We postulate the existence of a second type of G-cell that represents spatial attention by modulating the activity of all BOS cells in a spatially defined area. Simulations of this model show that a combination of spatial and object-based mechanisms fully accounts for the observed pattern of synchrony between BOS neurons. Our results suggest that modulatory feedback from G-cells may underlie both spatial and object-based attention.

Attentional selection is a function that allocates the brain’s computational resources to the most important part of a visual scene at a specific moment. Saliency map models have been proposed as computational models to predict attentional selection within a spatial location. Recent saliency map models based on deep convolutional neural networks (DCNNs) exhibit the highest performance for predicting the location of attentional selection and human gaze, which reflect overt attention. Trained DCNNs potentially provide insight into the perceptual mechanisms of biological visual systems. However, the relationship between artificial and neural representations used for determining attentional selection and gaze location remains unknown. To understand the mechanism underlying saliency map models based on DCNNs and the neural system of attentional selection, we investigated the correspondence between layers of a DCNN saliency map model and monkey visual areas for natural image representations. We compared the characteristics of the responses in each layer of the model with those of the neural representation in the primary visual (V1), intermediate visual (V4), and inferior temporal cortices. Regardless of the DCNN layer level, the characteristics of the responses were consistent with that of the neural representation in V1. We found marked peaks of correspondence between V1 and the early level and higher-intermediate-level layers of the model. These results provide insight into the mechanism of the trained DCNN saliency map model and suggest that the neural representations in V1 play an important role in computing the saliency that mediates attentional selection, which supports the V1 saliency hypothesis. Significance Statement Trained deep convolutional neural networks (DCNNs) potentially provide insight into the perceptual mechanisms of biological visual systems. However, the relationship between artificial and neural representations for determining attentional selection and gaze location has not been identified. We compared the characteristics of the responses in each layer of a DCNN model for predicting attentional selection with those of the neural representation in visual cortices. We found that the characteristics of the responses in the trained DCNN model for attentional selection were consistent with that of the representation in the primary visual cortex (V1), suggesting that the activities in V1 underlie the neural representations of saliency in the visual field to exogenously guide attentional selection. This study supports the V1 saliency hypothesis.