Subcortical connectivity correlates selectively with attention’s effects on spatial choice bias

Abstract

Neural mechanisms of attention are extensively studied in the neocortex; comparatively little is known about how subcortical regions contribute to attention. The superior colliculus (SC) is an evolutionarily conserved, subcortical (midbrain) structure that has been implicated in controlling visuospatial attention. Yet how the SC contributes mechanistically to attention remains unknown. We investigated the role of the SC in attention, combining model-based psychophysics, diffusion imaging, and tractography in human participants. Specifically, we asked whether the SC contributes to enhancing sensitivity (d′) to attended information, or whether it contributes to biasing choices (criteria) in favor of attended information. We tested human participants on a multialternative change detection task, with endogenous spatial cueing, and quantified sensitivity and bias with a recently developed multidimensional signal detection model (m-ADC model). At baseline, sensitivity and bias exhibited complementary patterns of asymmetries across the visual hemifields: While sensitivity was consistently higher for detecting changes in the left hemifield, bias was higher for reporting changes in the right hemifield. Remarkably, white matter connectivity of the SC with the neocortex mirrored this pattern of asymmetries. Specifically, the asymmetry in SC–cortex connectivity correlated with the asymmetry in choice bias, but not in sensitivity. In addition, SC–cortex connectivity strength could predict cueing-induced modulation of bias, but not of sensitivity, across individuals. In summary, the SC may be a key node in an evolutionarily conserved network for controlling choice bias during visuospatial attention.

Visual selective attention and the control of tracking eye movements: a critical review

“…One possibility is that SC activity biases response choice without impacting sensory processing, as can be said of the effect of cueing on behavioral responses (6). A reanalysis of prior microstimulation studies within a signal detection framework ( 122), an analysis of interindividual differences in functional connectivity (fMRI) in the human (154), and correlations between SC activity and shifts in response criteria (20), suggest that the SC activity may impact target choice by shifting response criteria in favor of precued target locations, without generating a spatial bias in the global competition for sensory representation as suggested above (e.g., 116).…”

“…However, SC inactivation had no measurable effect on the cue-related attentional modulation observed in MST and MT, meaning that visual information must have been prioritized via alternative pathways, which do not involve the amplification of firing rates (115). Sreenivasan and Sridharan (154) suggested that in the human brain, there is no need to find such alternative pathways because the SC only affects target choice. In the monkey brain, however, recent inactivation studies using a paradigm to separate shifts in criterion from shifts in sensitivity (122,156) indicate the SC does enhance sensitivity in the task.…”

Attention in Psychology, Neuroscience, and Machine Learning

“…Finally, some forms of attention appear to act in multiple ways on the same system. For example, visual attention is believed to both: (1) enhance the sensitivity of visual neurons in the cortex by modulating their activity and (2) change subcortical activity such that sensory information is readout differently (Birman and Gardner, 2019;Sreenivasan and Sridharan, 2019). In this way, attention uses two different mechanisms, in different parts of the brain, to create its effect.…”

Same, same but different? A multi-method review of the processes underlying executive control.

“…Studies performed in non-human primates have also shown that the pulvinar (in the posterior thalamus and strongly connected with visual occipital regions), is involved in coordinating functional interactions across cortical areas for visual attention (Saalmann et al, 2012;Zhou et al, 2016). This region is also connected with the superior colliculus, a midbrain structure that enables both stimulus-driven and goal-driven attention across species (Friedrich et al, 2020;V. Sreenivasan & Sridharan, 2019).…”