Neuronal Basis of Covert Spatial Attention in the Frontal Eye Field

Abstract

The influential "premotor theory of attention" proposes that developing oculomotor commands mediate covert visual spatial attention. A likely source of this attentional bias is the frontal eye field (FEF), an area of the frontal cortex involved in converting visual information into saccade commands. We investigated the link between FEF activity and covert spatial attention by recording from FEF visual and saccade-related neurons in monkeys performing covert visual search tasks without eye movements. Here we show that the source of attention signals in the FEF is enhanced activity of visually responsive neurons. At the time attention is allocated to the visual search target, nonvisually responsive saccade-related movement neurons are inhibited. Therefore, in the FEF, spatial attention signals are independent of explicit saccade command signals. We propose that spatially selective activity in FEF visually responsive neurons corresponds to the mental spotlight of attention via modulation of ongoing visual processing.

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).…”

Toward enhanced P300 speller performance

“…Secondly, spatial attention involves both overt eye gaze and covert processes. Covert visuospatial attention has been shown to modulate neuronal activity [22] and ERP components [15]. Thus, definitive information on the relative contribution of overt eye movements to the P300 speller performance will require either studies controlling for the effect of eye movements or studies with individuals lacking voluntary control of eye movements.…”

The Premotor theory of attention: Time to move on?

“…These data are often interpreted as evidence of functional equivalence between saccade preparation and covert attention. However, this interpretation of data from the FEF is problematic for the following reason; FEF contains multiple overlapping but independent neuronal populations, some of which are involved in visual selection but not motor control, and others that are involved in saccade control but not visual attention (Sato & Schall, 2003;Thompson, Bichot, & Schall, 1997;Thompson, Biscoe, & Sato, 2005). In other words, contrary to the predictions of the Premotor theory, the FEF neurons that drive saccadic eye-movements are separate from the neurons that drive visual selection.…”

“…There is evidence that activating monkey FEF using microstimulation is sufficient to bias attention (Armstrong et al, 2006;Armstrong & Moore, 2007;Moore & Fallah, 2001), but this bias is unlikely to originate from the specific activation of neurons involved in motor preparation as compelling neurophysiological evidence suggests that covert attention and saccade control are mediated by separate neuronal populations in FEF (Juan et al, 2008;Juan et al, 2004;Sato & Schall, 2003;Thompson et al, 1997;Thompson et al, 2005). Furthermore, it is probable that the perceptual enhancements observed at saccade goals prior to saccade execution are driven by the mechanisms which ensure the maintenance of perceptual stability which do not operate when no saccade is executed (Duhamel et 30 al., 1992;Khan et al, 2009).…”