Late Development of Cue Integration Is Linked to Sensory Fusion in Cortex

Adults optimize perceptual judgements by integrating different types of sensory information [1Hillis J.M. Watt S.J. Landy M.S. Banks M.S. Slant from texture and disparity cues: optimal cue combination.J. Vis. 2004; 4: 967-992Crossref PubMed Scopus (340) Google Scholar, 2Ernst M.O. Banks M.S. Humans integrate visual and haptic information in a statistically optimal fashion.Nature. 2002; 415: 429-433Crossref PubMed Scopus (3062) Google Scholar]. This engages specialized neural circuits that fuse signals from the same [3Ban H. Preston T.J. Meeson A. Welchman A.E. The integration of motion and disparity cues to depth in dorsal visual cortex.Nat. Neurosci. 2012; 15: 636-643Crossref PubMed Scopus (77) Google Scholar, 4Dövencioğlu D. Ban H. Schofield A.J. Welchman A.E. Perceptual integration for qualitatively different 3-D cues in the human brain.J. Cogn. Neurosci. 2013; 25: 1527-1541Crossref PubMed Scopus (22) Google Scholar, 5Murphy A.P. Ban H. Welchman A.E. Integration of texture and disparity cues to surface slant in dorsal visual cortex.J. Neurophysiol. 2013; 110: 190-203Crossref PubMed Scopus (36) Google Scholar] or different [6Gu Y. Angelaki D.E. Deangelis G.C. Neural correlates of multisensory cue integration in macaque MSTd.Nat. Neurosci. 2008; 11: 1201-1210Crossref PubMed Scopus (385) Google Scholar] modalities. Whereas young children can use sensory cues independently, adult-like precision gains from cue combination only emerge around ages 10 to 11 years [7Nardini M. Jones P. Bedford R. Braddick O. Development of cue integration in human navigation.Curr. Biol. 2008; 18: 689-693Abstract Full Text Full Text PDF PubMed Scopus (293) Google Scholar, 8Gori M. Del Viva M. Sandini G. Burr D.C. Young children do not integrate visual and haptic form information.Curr. Biol. 2008; 18: 694-698Abstract Full Text Full Text PDF PubMed Scopus (357) Google Scholar, 9Nardini M. Bedford R. Mareschal D. Fusion of visual cues is not mandatory in children.Proc. Natl. Acad. Sci. USA. 2010; 107: 17041-17046Crossref PubMed Scopus (101) Google Scholar]. Why does it take so long to make best use of sensory information? Existing data cannot distinguish whether this (1) reflects surprisingly late changes in sensory processing (sensory integration mechanisms in the brain are still developing) or (2) depends on post-perceptual changes (integration in sensory cortex is adult-like, but higher-level decision processes do not access the information) [10Kiorpes L. Visual development in primates: neural mechanisms and critical periods.Dev. Neurobiol. 2015; 75: 1080-1090Crossref PubMed Scopus (39) Google Scholar]. We tested visual depth cue integration in the developing brain to distinguish these possibilities. We presented children aged 6–12 years with displays depicting depth from binocular disparity and relative motion and made measurements using psychophysics, retinotopic mapping, and pattern classification fMRI. Older children (>10.5 years) showed clear evidence for sensory fusion in V3B, a visual area thought to integrate depth cues in the adult brain [3Ban H. Preston T.J. Meeson A. Welchman A.E. The integration of motion and disparity cues to depth in dorsal visual cortex.Nat. Neurosci. 2012; 15: 636-643Crossref PubMed Scopus (77) Google Scholar, 4Dövencioğlu D. Ban H. Schofield A.J. Welchman A.E. Perceptual integration for qualitatively different 3-D cues in the human brain.J. Cogn. Neurosci. 2013; 25: 1527-1541Crossref PubMed Scopus (22) Google Scholar, 5Murphy A.P. Ban H. Welchman A.E. Integration of texture and disparity cues to surface slant in dorsal visual cortex.J. Neurophysiol. 2013; 110: 190-203Crossref PubMed Scopus (36) Google Scholar]. By contrast, in younger children (<10.5 years), there was no evidence for sensory fusion in any visual area. This significant age difference was paired with a shift in perceptual performance around ages 10 to 11 years and could not be explained by motion artifacts, visual attention, or signal quality differences. Thus, whereas many basic visual processes mature early in childhood [11Norcia A.M. Tyler C.W. Spatial frequency sweep VEP: visual acuity during the first year of life.Vision Res. 1985; 25: 1399-1408Crossref PubMed Scopus (338) Google Scholar, 12Braddick O.J. Atkinson J. Infants’ sensitivity to motion and temporal change.Optom. Vis. Sci. 2009; 86: 577-582Crossref PubMed Scopus (18) Google Scholar], the brain circuits that fuse cues take a very long time to develop.