Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas

PLoS Biol. 2017 Nov 30;15(11):e2003646. doi: 10.1371/journal.pbio.2003646. eCollection 2017 Nov.

Abstract

Rapidly grouping local elements into an organized object (i.e., perceptual integration) is a fundamental yet challenging task, especially in noisy contexts. Previous studies demonstrate that ventral visual pathway, which is widely known to mediate object recognition, engages in the process by conveying object-level information processed in high-level areas to modulate low-level sensory areas. Meanwhile, recent evidence suggests that the dorsal visual pathway, which is not typically attributable to object recognition, is also involved in the process. However, the underlying whole-brain fine spatiotemporal neuronal dynamics remains unknown. Here we used magnetoencephalography (MEG) recordings in combination with a temporal response function (TRF) approach to dissociate the time-resolved neuronal response that specifically tracks the perceptual grouping course. We demonstrate that perceptual integration initiates robust and rapid responses along the dorsal visual pathway in a reversed hierarchical manner, faster than the ventral pathway. Specifically, the anterior intraparietal sulcus (IPS) responds first (i.e., within 100 ms), followed by activities backpropagating along the dorsal pathway to early visual areas (EVAs). The IPS activity causally modulates the EVA response, even when the global form information is task-irrelevant. The IPS-to-EVA response profile fails to appear when the global form could not be perceived. Our results support the crucial function of the dorsal visual pathway in perceptual integration, by quickly extracting a coarse global template (i.e., an initial object representation) within first 100 ms to guide subsequent local sensory processing so that the ambiguities in the visual inputs can be efficiently resolved.

MeSH terms

  • Adult
  • Brain Mapping / methods
  • Female
  • Humans
  • Magnetic Resonance Imaging / methods
  • Magnetoencephalography
  • Male
  • Pattern Recognition, Visual / physiology*
  • Photic Stimulation / methods
  • Visual Cortex / physiology*
  • Visual Pathways*
  • Visual Perception / physiology*
  • Young Adult

Grants and funding

National Natural Science Foundation of China (grant number 31522027 and 31571115). Received by H.L.. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Guangdong Pearl River Talents Plan Innovative and Entrepreneurial Team grant (grant number 2016ZT06S220). Received by K.Z.. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Natural Science Foundation of China (grant number 31671133). Received by K.Z.. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Key Basic Research Program of China (grant number 2015CB351701). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.