Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention

Author summary Vision allows us to make sense out of a very complex signal, the patterns of light rays reaching our eyes. Two mechanisms are essential for this: perceptual organization which structures the input into meaningful visual objects, and attention which selects only the most important parts in the input. Prior work suggests that both of these mechanisms are implemented by neurons called grouping cells. These organize the object features into coherent entities (perceptual grouping) and access them as needed (selective attention). For technical reasons it is difficult to observe grouping cells but their effect can be seen in the influence they have on responses of other classes of cells. These responses have been measured experimentally and it was found that they depend in unexpected ways on where the subject was attending. Using a computational model, we here demonstrate that the responses can be understood in terms of the interaction between two kinds of selective attention, both of which are known to occur in primate perception. One is attention to a specific area in the environment, the other is to specific objects. A model including both of these attentional mechanisms generates neuronal responses in agreement with the observed patterns of neural activity. 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.