Contextual Feedback to Superficial Layers of V1
Neuronal cortical circuitry comprises feedforward, lateral, and feedback projections, each of which terminates in distinct cortical layers [1Larkum M. A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex.Trends Neurosci. 2013; 36: 141-151Abstract Full Text Full Text PDF PubMed Scopus (399) Google Scholar, 2Markov N.T. Vezoli J. Chameau P. Falchier A. Quilodran R. Huissoud C. Lamy C. Misery P. Giroud P. Ullman S. et al.Anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex.J. Comp. Neurol. 2014; 522: 225-259Crossref PubMed Scopus (364) Google Scholar, 3Sillito A.M. Cudeiro J. Jones H.E. Always returning: feedback and sensory processing in visual cortex and thalamus.Trends Neurosci. 2006; 29: 307-316Abstract Full Text Full Text PDF PubMed Scopus (188) Google Scholar]. In sensory systems, feedforward processing transmits signals from the external world into the cortex, whereas feedback pathways signal the brain’s inference of the world [4Bastos A.M. Usrey W.M. Adams R.A. Mangun G.R. Fries P. Friston K.J. Canonical microcircuits for predictive coding.Neuron. 2012; 76: 695-711Abstract Full Text Full Text PDF PubMed Scopus (1177) Google Scholar, 5Bullier J. Integrated model of visual processing.Brain Res. Brain Res. Rev. 2001; 36: 96-107Crossref PubMed Scopus (747) Google Scholar, 6Clark A. Whatever next? Predictive brains, situated agents, and the future of cognitive science.Behav. Brain Sci. 2013; 36: 181-204Crossref PubMed Scopus (2520) Google Scholar, 7Gilbert C.D. Sigman M. Brain states: top-down influences in sensory processing.Neuron. 2007; 54: 677-696Abstract Full Text Full Text PDF PubMed Scopus (594) Google Scholar, 8Meyer K. Another remembered present.Science. 2012; 335: 415-416Crossref PubMed Scopus (11) Google Scholar, 9Muckli L. Petro L.S. Network interactions: non-geniculate input to V1.Curr. Opin. Neurobiol. 2013; 23: 195-201Crossref PubMed Scopus (86) Google Scholar, 10Mumford D. On the computational architecture of the neocortex. II. The role of cortico-cortical loops.Biol. Cybern. 1992; 66: 241-251Crossref PubMed Scopus (752) Google Scholar, 11Park H.J. Friston K. Structural and functional brain networks: from connections to cognition.Science. 2013; 342: 1238411Crossref PubMed Scopus (1100) Google Scholar]. However, the integration of feedforward, lateral, and feedback inputs within each cortical area impedes the investigation of feedback, and to date, no technique has isolated the feedback of visual scene information in distinct layers of healthy human cortex. We masked feedforward input to a region of V1 cortex and studied the remaining internal processing. Using high-resolution functional brain imaging (0.8 mm3) and multivoxel pattern information techniques, we demonstrate that during normal visual stimulation scene information peaks in mid-layers. Conversely, we found that contextual feedback information peaks in outer, superficial layers. Further, we found that shifting the position of the visual scene surrounding the mask parametrically modulates feedback in superficial layers of V1. Our results reveal the layered cortical organization of external versus internal visual processing streams during perception in healthy human subjects. We provide empirical support for theoretical feedback models such as predictive coding [10Mumford D. On the computational architecture of the neocortex. II. The role of cortico-cortical loops.Biol. Cybern. 1992; 66: 241-251Crossref PubMed Scopus (752) Google Scholar, 12Friston K. A theory of cortical responses.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005; 360: 815-836Crossref PubMed Scopus (2475) Google Scholar] and coherent infomax [13Phillips W.A. Clark A. Silverstein S.M. On the functions, mechanisms, and malfunctions of intracortical contextual modulation.Neurosci. Biobehav. Rev. 2015; 52: 1-20Crossref PubMed Scopus (46) Google Scholar] and reveal the potential of high-resolution fMRI to access internal processing in sub-millimeter human cortex.