Attention and Capacity Limits in Perception: A Cellular Metabolism Account

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.

Regional Haemodynamic and Metabolic Coupling in Infants

“…This might indicate distinct spatial localisation of the cytochrome response in comparison to the haemodynamics. Studies have demonstrated that task-related increases in oxidative metabolism and energy demand were smaller (approximately 15%) in comparison to the increase in CBF (approximately 60%) (Lin et al, 2010;Bruckmaier et al, 2020), which could potentially explain the fewer number of channels activated for oxCCO. Indeed, previous studies have suggested that oxygen consumption is more spatially specific in comparison to changes in cerebral blood flow (Malonek and Grinvald, 1996).…”

Alpha oscillations reflect suppression of distractors with increased perceptual load

“…BOLD responses are typically negatively correlated with alpha band power [39][40][41] . Similarly, using spectroscopy, Bruckmaier et al 14 recently showed increased cellular metabolism for attended target and a reduction for unattended stimuli with increased perceptual load. The current results thus provide evidence that the previously observed resource reduction for the distractor due to a target load increase is implemented by an increase in alpha band power.…”

“…As alpha band oscillations have been shown to reflect functional inhibition 12,13 , the primary role of alpha oscillations is thought to be the suppression of the processing pathway of the irrelevant items as well as engaging the attended pathway by a decrease in alpha power. Perceptual load theory predicts a reduction of resources for distractors with increased target processing load 14 . However, it remains unclear how the theory relates to modulations in the alpha band.…”

Inattentive Perception, Time, and the Incomprehensibility of Consciousness

“…Even a brief interval above average energy levels in a limited cerebral region needs to be balanced out by reductions in metabolism elsewhere (Clarke and Sokoloff, 1999 ). Lennie ( 2003 ) writes: “Even with only a few percent of neurons concurrently active in any local region, the metabolic burden would be unsustainable over all of cortex.” A consequence of this is that, if attention is devoted to a visual discrimination task, processing capacity is lower for other unattended processes (Bruckmaier et al, 2020 ). Since inattentive visual processes constitute by far the largest part of total perceptual content (see below), energy considerations make it unlikely that inattentive perception is mediated by current neuronal activity.…”