Descending Control of Neural Bias and Selectivity in a Spatial Attention Network: Rules and Mechanisms

Abstract

The brain integrates stimulus-driven (exogenous) activity with internally generated (endogenous) activity to compute the highest priority stimulus for gaze and attention. Little is known about how this computation is accomplished neurally. We explored the underlying functional logic in a critical component of the spatial attention network, the optic tectum (OT, superior colliculus in mammals), in awake barn owls. We found that space-specific endogenous influences, evoked by activating descending forebrain pathways, bias competition among exogenous influences, and substantially enhance the quality of the categorical neural pointer to the highest priority stimulus. These endogenous influences operate across sensory modalities. Biologically grounded modeling revealed that the observed effects on network bias and selectivity require a simple circuit mechanism: endogenously driven gain modulation of feedback inhibition among competing channels. Our findings reveal fundamental principles by which internal and external information combine to guide selection of the next target for gaze and attention.