Testing sensory evidence against mnemonic templates

Abstract

Most perceptual decisions require comparisons between current input and an internal template. Classic studies propose that templates are encoded in sustained activity of sensory neurons. However, stimulus encoding is itself dynamic, tracing a complex trajectory through activity space. Which part of this trajectory is pre-activated to reflect the template? Here we recorded magneto- and electroencephalography during a visual target-detection task, and used pattern analyses to decode template, stimulus, and decision-variable representation. Our findings ran counter to the dominant model of sustained pre-activation. Instead, template information emerged transiently around stimulus onset and quickly subsided. Cross-generalization between stimulus and template coding, indicating a shared neural representation, occurred only briefly. Our results are compatible with the proposal that template representation relies on a matched filter, transforming input into task-appropriate output. This proposal was consistent with a signed difference response at the perceptual decision stage, which can be explained by a simple neural model.

DOI: http://dx.doi.org/10.7554/eLife.09000.001

eLife digest

Imagine searching for your house keys on a cluttered desk. Your eyes scan different items until they eventually find the keys you are looking for. How the brain represents an internal template of the target of your search (the keys, in this example) has been a much-debated topic in neuroscience for the past 30 years. Previous research has indicated that neurons specialized for detecting the sought-after object when it is in view are also pre-activated when we are seeking it. This would mean that these ‘template’ neurons are active the entire time that we are searching.

Myers et al. recorded brain activity from human volunteers using a non-invasive technique called magnetoencephalography (MEG) as they tried to detect when a particular shape appeared on a computer screen. The patterns of brain activity could be analyzed to identify the template that observers had in mind, and to trace when it became active. This revealed that the template was only activated around the time when a target was likely to appear, after which the activation pattern quickly subsided again.

Myers et al. also found that holding a template in mind largely activated different groups of neurons to those activated when seeing the same shape appear on a computer screen. This is contrary to the idea that the same cells are responsible both for maintaining a template and for perceiving its presence in our surroundings.

The brief activation of the template suggests that templates may come online mainly to filter new sensory evidence to detect targets. This mechanism could be advantageous because it lowers the amount of neural activity (and hence energy) needed for the task. Although this points to a more efficient way in which the brain searches for targets, these findings need to be replicated using other methods and task settings to confirm whether the brain generally uses templates in this way.

DOI: http://dx.doi.org/10.7554/eLife.09000.002