Microstimulation of the superior colliculus focuses attention without moving the eyes

Abstract

The superior colliculus (SC) is part of a network of brain areas that directs saccadic eye movements, overtly shifting both gaze and attention from position to position, in space. Here, we seek direct evidence that the SC also contributes to the control of covert spatial attention, a process that focuses attention on a region of space different from the point of gaze. While requiring monkeys to keep their gaze fixed, we tested whether microstimulation of a specific location in the SC spatial map would enhance visual performance at the corresponding region of space, a diagnostic measure of covert attention. We find that microstimulation improves performance in a spatially selective manner: thresholds decrease at the location in visual space represented by the stimulated SC site, but not at a control location in the opposite hemifield. Our data provide direct evidence that the SC contributes to the control of covert spatial attention. discrimination ͉ psychophysics S everal lines of evidence suggest that eye movements and covert attention may be mediated by the same neural mechanisms (1-3). For example, a human subject can direct attention to a specific location in space, thereby gaining a measurable advantage in visual performance, even while maintaining fixation at an altogether different location (4). During a saccadic eye movement, however, the subject is unable to direct attention to any location other than the endpoint of that eye movement (5).In the monkey, electrophysiological experiments have increasingly implicated eye-movement planning structures in the control of covert spatial attention. Following the original observation by Goldberg and Wurtz (6) of attention-related neural activity in the superior colliculus (SC) (7, 8), single-unit recordings have detected attentional effects in other eye movementrelated areas of the brain, including the inferior parietal cortex (9-11) and the frontal eye fields (FEF) (12)(13)(14). Recent studies by Bisley and Goldberg (15) in the lateral intraparietal area and by Ignashchenkova et al. (16) in the SC were particularly incisive because the neural effects correlated parametrically with variations in the strength and timing of attentional effects in the behavioral data. Electrophysiological evidence, however, is necessarily correlative and cannot demonstrate that neural activity causes behavior (17).Remarkable studies published recently by Moore and Fallah (18,19) bridged this gap. Using visual threshold measurements as a behavioral metric of attention, they showed that electrical microstimulation of the FEF improved psychophysical performance by facilitating the deployment of attention to the location of the visual stimulus. The effect was spatially localized to the region of the visual field encoded at the stimulation site and thus could not be attributed to a general increase in arousal or vigilance. This was a landmark study first because of its implications concerning the neural substrate of visuo-spatial attention, but more importantly because it is the only d...

Drivers from the deep: the contribution of collicular input to thalamocortical processing

“…It is inferred that the SC stimulation affects visual processing in the cortex since the determination of direction of visual motion (the basis of the change blindness task) depends on identified areas of visual cortex, specifically extrastriate area MT (Newsome et al, 1985;Newsome and Pare, 1988). A recent report by Mu¨ller et al (2005) appeared to confirm this.…”

Differential Influence of Attention on Gaze and Head Movements

“…It has been established that saccade execution requires a shift of attention to the saccade goal (e.g., Deubel and Schneider 1996;Hoffman and Subramaniam 1995;Kowler et al 1995;McPeek et al 1999), indicating a close linkage between eye movements and attention. Such a linkage is also supported by a number of studies showing shared neural substrates for saccadic eye movement planning and attentional processing (e.g., Beauchamp et al 2001;Cavanaugh and Wurtz 2004;Corbetta et al 1998;Goldberg et al 2006;Ignashchenkova et al 2004;Kastner and Ungerleider 2000;Moore and Fallah 2001;Muller et al 2005; Thompson et al 2005). In addition, exogenous attentional cueing of a saccade target position before target presentation can facilitate or inhibit responses to the target, resulting in modulations of saccade latencies (e.g., Dorris et al 2002;Fecteau and Munoz 2006;Posner et al 1982).…”

“…Many regions known to be involved in saccadic eye movements and attention (Cavanaugh and Wurtz 2004;Corbetta et al 1998;Ignashchenkova et al 2004;Krauzlis 2004Krauzlis , 2005McPeek 2006McPeek , 2008Moore and Fallah 2001;Muller et al 2005;Pierrot-Deseilligny et al 2004;Thompson et al 2005;Wardak et al 2006) are also involved in combined eye-head movements. These include the frontal eye fields (Chen 2006;Elsley et al 2007;Knight and Fuchs 2007;Monteon et al 2005;Tu and Keating 2000;van der Steen et al 1986), the supplementary eye fields (Chen and Walton 2005;MartinezTrujillo et al 2003MartinezTrujillo et al , 2004, and the superior colliculus (Freedman and Sparks 1997a;Freedman et al 1996;Klier et al 2001;Martinez-Trujillo et al 2003;Walton et al 2007Walton et al , 2008.…”

Stimulus-specific adaptation, habituation and change detection in the gaze control system

“…The above-mentioned hypothesis is supported by numerous electrophysiological studies demonstrating that neurons in the OT/SC are sensitive to the saliency of the stimulus inside their receptive field (for example: Horwitz and Newsome 1999;McPeek and Keller 2002;Pluta et al 2011). Further evidence for the causal role of the SC in stimulus selection and spatial attention was provided by several inactivation and microstimulation studies (Muller et al 2005;Lovejoy and Krauzlis 2009). Of particular interest to this prospect is a series of recent studies in barn owls addressing mechanisms of competitive stimulus selection in the OT Mysore et al , 2010Lai et al 2011).…”