attention without consciousness

From Scholarpedia

Curator: Dr. Naotsugu Tsuchiya, California Institute of Technology, Pasadena, CA, USA
Curator: Dr. Christof Koch, Division of Biology, Caltech, Pasadena, CA

Attention without consciousness

Processing of invisible stimulus requires top-down attention

In lateral masking (visual crowding), the orientation of a peripherally-presented grating is hidden from conscious sight but remains sufficiently potent to induce an orientation-dependent aftereffect (He et al., 1996). In this case, the orientation of the grating is not consciously accessible to the subject yet something is still seen at that location (that is, in this case only some attributes of the object are invisible). Montaser-Kouhsari and Rajimehr (2004) showed that an aftereffect induced by an invisible illusory contour required focal attention to the aftereffect-inducing object, even though the attribute of that object at the center of attention was invisible. Naccache and colleagues (Naccache et al., 2002) elicited priming for invisible words (suppressed by a combination of forward and backward masking) but only if the subject was attending to the invisible prime-target pair; without attention, the same word failed to elicit priming. In both cases, attentional selection of a spatial location and its contents was necessary to obtain the aftereffect or priming even though the relevant attribute (orientation, letter to identify) was invisible.

Invisible stimulus attracts spatial attention

Male/female nudes attracted attention and induced involuntary eye movements when they were rendered completely invisible by continuous flash suppression (Feng et al., 2006; Jiang et al., 2006). Interestingly, in heterosexuals, these effects were only apparent for nudes of the opposite sex (see also (McCormick, 1997; Rajimehr, 2004; Sumner et al., 2006)). Note that by themselves (i.e. without the mask), these stimuli are clearly visible.

Likewise, the blindsight patient GY has the usual reaction-time advantages for the detection of targets in his blind visual field when attentionally cued, even when the cues are located in his blind field and are therefore invisible to him (Kentridge et al., 1999a, 1999b, 2004).

Feature-based attention can spread to invisible target

Feature-based attention can spread to invisible stimuli (Melcher et al., 2005; Kanai et al., 2006). Indeed, when searching for an object in a cluttered scene (e.g., keys in a messy room), attention is paid to an invisible object and its associated features.

Imaging attention to invisible stimulus

Figure 1: Object images presented to the periphery of the non-dominant eye are rendered invisible by continuous flash suppression (CFS) at the corresponding and two other locations in the dominant eye. Modified from (Bahrami et al., 2007) with permission.

Figure 2: At the center of the display, subjects performed a rapid serial visual presentation (RSVP) task. In the low load condition, a target letter "T" of white or black color must be detected. In the high load condition, either a "white N" or a "black Z" must be detected, embedded within a stream of letters. Modified from (Bahrami et al., 2007) with permission.

Figure 3: fMRI response amplitude in primary visual cortex to invisible objects is modulated by the attention load on the central task. Modified from (Bahrami et al., 2007) with permission.

Spatial attention modulates the processing of invisible stimuli

More direct evidence comes from a recent fMRI study by Bahrami and colleagues (Bahrami et al., 2007), demonstrating that the processing of objects hidden from sight (with d’ = 0) via continuous flash suppression (Tsuchiya and Koch, 2005) depended on the availability of spatial attention (Figs.1,2,3). They varied the load of the central task in a dual-task design Attention and Consciousness/How to manipulate attention. The hemodynamic blood-oxygen-level-dependent contrast (BOLD) response to the invisible objects in primary visual cortex, V1, was stronger when the central task was easy, that is, when spatial attention was available for processing the invisible, peripheral stimulus than when the central task was hard and more attentional resources were drawn to it. In other words, available attentional capacity modulated the fMRI response to an invisible stimulus.

Subthreshold motion is more distracting than suprathreshold motion

Figure 4: Subthreshold motion is more distracting than suprathreshold motion. (A) Subjects had to detect two target digits embedded in a rapid stream of letters (RSVP). Surrounding the letter stream, moving random dots of variable coherence were presented. (B) The central RSVP task performance (on the y-axis) dropped when the peripheral motion was below threshold for detecting coherent motion. Note that stronger motion (i.e., higher coherency) did not interfere with the central task. (C) Activation of the cortical region MT+ was highest when peripheral motion was below threshold. (D) Activation of lateral prefrontal cortex (LPFC), which inhibits activity in MT+, was higher when motion coherence was above the threshold. Subthreshold motion does not activate LPFC. Modified from (Tsushima et al., 2006) with permission.

An even more paradoxical effect - that invisible stimuli can be more distracting than visible ones – was discovered by Tsushima and colleagues (Tsushima et al., 2006) (Fig.4A). In this study, subjects had to detect foveally-placed targets in a stream of characters – a rapid serial visual presentation (RSVP) task - surrounded by an annulus of moving dots. The fraction of dots moving coherently in one direction – the motion coherence - was varied from 0% (truly random dot motion) to 50% (half of the dots move in the same direction). When the central task was combined with the task-irrelevant surround motion, the central performance dropped when the coherent motion was perceptually below threshold (say at 5%, where the cloud of dots was not perceived to move coherently) compared to when the motion coherence was 0% or above threshold (e.g., 20%) (Fig.4B). This counterintuitive finding was explained by the parallel fMRI study in which the authors looked at BOLD activity in area MT+, which reflects the degree of distraction by motion stimuli, and in the lateral prefrontal cortex (LPFC), which provides an attentional suppression signal to MT+ (Fig.4CD). Compatible with the behavioral findings, invisible motion did not elicit activity in the LPFC, resulting in higher distractor-related activity in MT+. On the other hand, visible motion evoked a stronger LPFC signal but a weaker MT+ one. The authors hypothesize that invisible motion activates MT+, impairing performance, but not the LPFC, which fails to inhibit MT+; thereby stimuli that are not consciously perceived can escape inhibitory control, a phenomenon more familiar from psychoanalysis than from sensory psychology.

References

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• Kanai R, Tsuchiya N, Verstraten FA (2006) The scope and limits of top-down attention in unconscious visual processing. Curr Biol.
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• Sumner P, Tsai PC, Yu K, Nachev P (2006) Attentional modulation of sensorimotor processes in the absence of perceptual awareness. Proc Natl Acad Sci U S A 103:10520-10525.
• Tsuchiya N, Koch C (2005) Continuous flash suppression reduces negative afterimages. Nat Neurosci 8:1096-1101.
• Tsushima Y, Sasaki Y, Watanabe T (2006) Greater disruption due to failure of inhibitory control on an ambiguous distractor. Science 314:1786-1788.