Abstract
Limits on perceptual capacity result in various phenomena of inattentional blindness. Here we propose a neurophysiological account attributing these perceptual capacity limits directly to limits on cerebral cellular metabolism. We hypothesized that overall cerebral energy supply remains constant, regardless of overall mental processing demands; therefore, an attention mechanism is required to regulate limited cellular metabolism levels in line with attended task demands. Increased perceptual load in a task (imposing a greater demand on neural computations) should thus result in increased metabolism underlying attended processing, and reduced metabolism mediating unattended processing. We tested this prediction measuring oxidation states of cytochrome c oxidase (oxCCO), an intracellular marker of cellular metabolism. Broadband near-infrared spectroscopy was used to record oxCCO levels from human visual cortex while participants (both sexes) performed a rapid sequential visual search task under either high perceptual load (complex feature-conjunction search) or low load (feature pop-out search). A task-irrelevant, peripheral checkerboard was presented on a random half of trials. Our findings showed that oxCCO levels in visual cortex regions responsive to the attended-task stimuli were increased in high versus low perceptual load, whereas oxCCO levels related to unattended processing were significantly reduced. A negative temporal correlation of these load effects further supported our metabolism trade-off account. These results demonstrate an attentional compensation mechanism that regulates cellular metabolism levels according to processing demands. Moreover, they provide novel evidence for the widely held stipulation that overall cerebral metabolism levels remain constant regardless of mental task demand and establish a neurophysiological account for capacity limits in perception.SIGNIFICANCE STATEMENT We investigated whether capacity limits in perception can be explained by the effects of attention on the allocation of limited cellular metabolic energy for perceptual processing. We measured the oxidation state of cytochrome c oxidase, an intracellular measure of metabolism, in human visual cortex during task performance. The results showed increased levels of cellular metabolism associated with attended processing and reduced levels of metabolism underlying unattended processing when the task was more demanding. A temporal correlation between these effects supported an attention-directed metabolism trade-off. These findings support an account for inattentional blindness grounded in cellular biochemistry. They also provide novel evidence for the claim that cerebral processing is limited by a constant energy supply, which thus requires attentional regulation.
Highlights
Much research has demonstrated the limited nature of perceptual capacity, reporting that, in attention demanding tasks, observers can fail to perceive unattended objects, a phenomenon termed “inattentional blindness” (e.g., Simons and Chabris, 1999; Cartwright-Finch and Lavie, 2007)
The present results provide support for our proposed cellular metabolism account for perceptual capacity limits and the role of attention in perception
Higher perceptual load in the task was associated with increased cellular metabolism levels related to attended processing and reduced levels related to unattended processing in the form of a direct resource trade-off
Summary
Much research has demonstrated the limited nature of perceptual capacity, reporting that, in attention demanding tasks, observers can fail to perceive unattended objects, a phenomenon termed “inattentional blindness” (e.g., Simons and Chabris, 1999; Cartwright-Finch and Lavie, 2007). Neuroimaging research has attributed inattentional blindness to attentional modulations of visual cortex response to unattended stimuli (e.g., Rees et al, 1999). Schwartz et al, 2005; Torralbo et al, 2016), and in V4 and TEO in response to unattended, meaningful objects (e.g., flowers) (Pinsk et al, 2004). This pattern of findings was obtained across a variety of perceptual load manipulations, all known to increase the computational demand on perceptual capacity (Lavie, 2005; Whiteley and Sahani, 2012; Lavie et al, 2014). Behavioral reports demonstrated the analogous impact of perceptual load on conscious experience (e.g., Carmel et al, 2007; Macdonald and Lavie, 2008; Stolte et al, 2014)
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