Synchrony reveals object organization in early visual cortex

When we look at a scene, the visual system is very good at telling us where the interesting things are. It forms a fast sketch that includes a preliminary ordering of what is in front and what is behind. Identification of figure and ground is important in our ability to recognize objects, and the correct assignment of contours to regions that are identified as figures is critical. It remains an unresolved question in neuroscience how the brain represents objects. Theories have proposed that synchrony might encode how features relate to objects (von der Malsburg, 1986; Gray et al., 1989), or highlight information for selective processing (Niebur and Koch, 1994), but the evidence is controversial and the underlying mechanisms are largely unknown. I tested the hypothesis that synchrony is produced by shared feedback from grouping cells that specifically enhance the responses of neurons whose receptive fields fit the grouping templates. This mechanism is thought to instantiate proto-objects, the structure underlying object tracking and selective attention. I analyzed spike activity from pairs of neurons in areas VI and V2 of macaques performing an attention demanding task, and used border ownership selectivity (Zhou et al., 2000) to infer which grouping structure each neuron belonged to. My results confirm the specific predictions of the hypothesis: pairs of neurons that were classified as part of the same grouping structure showed significant synchrony when their common grouping structure was activated by an object that stimulated both neurons, whereas synchrony between neurons of different grouping structures was weak irrespective of the displayed objects. These findings are strong evidence for the existence of proto-object representations that provide a fast sketch of the location and rough shapes of potentially interesting objects in a visual scene.;The binding-by-synchrony hypothesis has recently been tested with powerful new paradigms that effectively varied the assignment of contour elements to objects (Lamme and Spekreijse, 1998; Roelfsema et al., 2004; Palanca and DeAngelis, 2005; Mihalas et al., 2007), but these studies found no evidence for the expected variation of synchrony. In contrast, several studies found support for a role of synchrony in coding visual attention (Fries et al., 2001; Womelsdorf and Fries, 2007). However, these studies demonstrated coherence of local field potentials, but did not show correlations between spike trains of neurons. This weakened the argument because the brain uses spike trains for communication, whereas field potentials are local (Xing et al., 2009; Katzner et al., 2009). Thus, to date, there has been no clear evidence for a role of synchrony in coding either binding or selective visual attention. I show that rather than being a general correlate of binding or selective attention, synchrony in the visual cortex predictively emerges within specific functional groups of neurons. My results indicate that synchrony is produced by mechanisms used by the system to detect and represent the object structure in sensory data.