Changes in perceptual sensitivity related to spatial cues depends on subcortical activity

Abstract

Spatial cues allow animals to selectively attend to relevant visual stimuli while ignoring distracters. This process depends on a distributed neuronal network, and an important current challenge is to understand the functional contributions made by individual brain regions within this network and how these contributions interact. Recent findings point to a possible anatomical segregation, with cortical and subcortical brain regions contributing to different functional components of selective attention. Cortical areas, especially visual cortex, may be responsible for implementing changes in perceptual sensitivity by changing the signal-tonoise ratio, whereas other regions, such as the superior colliculus, may be involved in processes that influence selection between competing stimuli without regulating perceptual sensitivity. Such a segregation of function would predict that when activity in the superior colliculus is suppressed by reversible inactivation, animals should still show changes in perceptual sensitivity mediated by the intact cortical circuits. Contrary to this prediction, here we report that inactivation of the primate superior colliculus eliminates the changes in perceptual sensitivity made possible by spatial cues. These findings demonstrate changes in perceptual sensitivity depend not only on neuronal activity in cortex but also require interaction with signals from the superior colliculus.attention | perception | sensitivity | superior colliculus | cortex S patial cues are known to improve perceptual sensitivity on visual discrimination and detection tasks, and these behavioral effects seem to originate from changes in neural activity across several brain regions (1). In monkey visual cortex, spatial cues change the statistics of neuronal activity, and these changes are thought to reflect an increase in signal-to-noise synonymous with the spatially restricted changes in perceptual sensitivity characteristic of selective attention (2-4). The frontal and parietal cortex are also strongly implicated in the control of spatial attention (2, 3). Electrical microstimulation of neurons in frontal cortex of monkeys leads to shifts in selective attention mimicking the effects of visual cues (5); conversely, suppression of neural activity in frontal or parietal cortex leads to deficits in performance on attention-demanding tasks (6-8).These and similar observations have led to an explanatory framework in which the fidelity of sensory processing in visual cortex is regulated by a network of frontal and parietal cortical areas (9-12). This framework predicts that suppression of activity in one or more of these areas should impair the ability of an animal to use cues to improve its perceptual sensitivity. This prediction has not been directly tested in animals, although clinical cases (13) and experiments in humans using transcranial magnetic stimulation (14, 15) corroborate the idea that these cortical areas are important for the orienting of attention and the use of spatial cues.In addition to this network o...

Attention-related modulation of caudate neurons depends on superior colliculus activity

“…When SC neuronal activity is perturbed by inactivation or microstimulation, performance in attention tasks is reliably altered in a spatially specific manner, even during covert tasks (Bogadhi et al, 2019;Bollimunta et al, 2018;Cavanaugh and Wurtz, 2004;Herman et al, 2018;Lovejoy and Krauzlis, 2010;Müller et al, 2005;Zénon and Krauzlis, 2012). During SC inactivation, improvements in perceptual sensitivity made possible by spatial cues are abolished (Lovejoy and Krauzlis, 2017). Despite SC inactivation preventing spatial cues from conferring a perceptual advantage, cue-related modulation of neuronal activity in extrastriate visual cortex remains robust during inactivation (Zénon and Krauzlis, 2012).…”

Dissecting Modulatory Effects of Visual Attention in Primate Lateral Prefrontal Cortex Using Signal Detection Theory

“…Interestingly, in a previous study using the same paradigm, the authors showed that neurons' firing rates in visual area V4 are modulated by shifts in d', but not in c (Luo and Maunsell, 2015). These results can be considered in conjunction with two recent studies in the superior colliculus (SC) (Lovejoy and Krauzlis, 2017;Sridharan et al, 2017). They found that SC contributes to attention through changes in both d' and c, with the latter being the dominant contribution.…”

Attention can be subdivided into neurobiological components corresponding to distinct behavioral effects

“…Recent studies from other laboratories support the idea that different brain structures have distinct relationships to behavioral changes in criterion and sensitivity (69,70). These reports focused on the SC, and, together, they indicate that neurons in the SC contribute to behavioral changes in either criterion or sensitivity, but with criterion being the more prominent component.…”