Scene complexity modulates degree of feedback activity during object detection in natural scenes

PLoS Comput Biol. 2018 Dec 31;14(12):e1006690. doi: 10.1371/journal.pcbi.1006690. eCollection 2018 Dec.

Abstract

Selective brain responses to objects arise within a few hundreds of milliseconds of neural processing, suggesting that visual object recognition is mediated by rapid feed-forward activations. Yet disruption of neural responses in early visual cortex beyond feed-forward processing stages affects object recognition performance. Here, we unite these discrepant findings by reporting that object recognition involves enhanced feedback activity (recurrent processing within early visual cortex) when target objects are embedded in natural scenes that are characterized by high complexity. Human participants performed an animal target detection task on natural scenes with low, medium or high complexity as determined by a computational model of low-level contrast statistics. Three converging lines of evidence indicate that feedback was selectively enhanced for high complexity scenes. First, functional magnetic resonance imaging (fMRI) activity in early visual cortex (V1) was enhanced for target objects in scenes with high, but not low or medium complexity. Second, event-related potentials (ERPs) evoked by target objects were selectively enhanced at feedback stages of visual processing (from ~220 ms onwards) for high complexity scenes only. Third, behavioral performance for high complexity scenes deteriorated when participants were pressed for time and thus less able to incorporate the feedback activity. Modeling of the reaction time distributions using drift diffusion revealed that object information accumulated more slowly for high complexity scenes, with evidence accumulation being coupled to trial-to-trial variation in the EEG feedback response. Together, these results suggest that while feed-forward activity may suffice to recognize isolated objects, the brain employs recurrent processing more adaptively in naturalistic settings, using minimal feedback for simple scenes and increasing feedback for complex scenes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Brain / physiology
  • Brain Mapping
  • Computational Biology
  • Electroencephalography
  • Evoked Potentials
  • Feedback, Physiological
  • Feedback, Psychological
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Models, Neurological*
  • Models, Psychological
  • Pattern Recognition, Visual / physiology*
  • Photic Stimulation
  • Reaction Time / physiology
  • Visual Cortex / physiology*
  • Young Adult

Grants and funding

This work is part of the Research Priority Program ‘Brain and Cognition’ at the University of Amsterdam. IIAG was supported by a Rubicon Fellowship from the Netherlands Organization for Scientific Research (NWO: https://www.nwo.nl/en) and VAFL was supported by an Advanced Investigator Grant from the European Research Council (ERC: http://erc.europa.eu/). SG was supported by the Dutch public-private research program COMMIT (http://www.commit-nl.nl). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.