Rebound Spiking as a Neural Mechanism for Surface Filling-in Hans Supèr 1,2,3 and August Romeo 1 Abstract ■ Perceptual filling-in is the phenomenon where visual informa- tion is perceived although information is not physically present. For instance, the blind spot, which corresponds to the retinal loca- tion where there are no photoreceptor cells to capture the visual signals, is filled-in by the surrounding visual signals. The neural mechanism for such immediate filling-in of surfaces is unclear. By means of computational modeling, we show that surround in- hibition produces rebound or after-discharge spiking in neurons that otherwise do not receive sensory information. The behavior of rebound spiking mimics the immediate surface filling-in illusion observed at the blind spot and also reproduces the filling-in of an empty object after a background flash, like in the color dove illu- sion. In conclusion, we propose rebound spiking as a possible neural mechanism for surface filling-in. ■ INTRODUCTION The blind spot is the region in the visual field that corre- sponds to the optic disk where the optic nerve leaves the retina. At this location, there are no light-detecting pho- toreceptor cells to capture the visual events, and conse- quently this part of the visual field is not perceived. Yet we do not see a hole in our visual scene when we look with one eye because the location of the blind spot is filled-in by the surrounding visual information (see Figure 1A). This is shown by neurophysiological reports that describe neural responses related to filling-in at the blind spot in the early visual cortex (Matsumoto & Komatsu, 2005; Komatsu, Kinoshita, & Murakami, 2000, 2002; Fiorani, Rosa, Gattas, & Rocha-Miranda, 1992), which are consistent with neural de- scriptions of other forms of surface filling-in early visual cor- tex (Huang & Paradiso, 2008; MacEvoy, Kim, & Paradiso, 1998; De Weerd, Gattass, Desimone, & Ungerleider, 1995). The neural mechanisms for filling-in of are still a matter of debate. Two different theories have been put forward to explain the filling-in completion phenomenon. One theory postulates that spreading of neural activity in early visual areas is the basis for filling-in of visual information (Pessoa, Thompson, & Noe, 1998; Ramachandran & Gregory, 1991). This theory is based on the assumption that cells at contrast borders spread their activity to surrounding cells. In such a case, filling-in is accomplished by the dense network of hori- zontal connections that exist in the visual cortex. Horizontal connections have slow conduction velocities (0.1–0.2 m/sec; Angelucci & Bressloff, 2006) and may explain slow surface filling-in processes but they are probably too slow to explain the rather immediate surface filling-in at the blind spot (see Komatsu, 2006). The other hypothesis, the cognitive or sym- bolic filling-in theory, postulates that blind regions are ig- nored and object representation is realized at high cortical level on the basis of contrast information from lower areas (Pessoa et al., 1998). Feedback projections from these higher areas have large axonal termination fields in the early visual areas and may so provide sensory information to neurons in the lower areas located at the blind spot region. However, it has been shown that feedback has a role in modulating stimulus-evoked responses and does not activate otherwise silent neurons (Ekstrom, Roelfsema, Arsenault, Bonmassar, & Vanduffel, 2008). This indicates that cortical neurons at the blind spot region need to be activated, presumably by feed-forward connections. How can retinal signals be effective in activating cells in early cortical areas that do not receive feed-forward exci- tatory projections? The excitatory retinal information is accompanied by inhibitory signals. Besides the global influ- ence, inhibition is robust, fast, and prominent in retina, LGN, and visual cortex (Alitto & Usrey, 2008; Solomon, Lee, & Sun, 2006; Blitz & Regehr, 2005). It is well known that strong inhibition may cause rebound excitation at the end of the hyperpolarized period. Rebound or paradoxical excitation is a biophysical feature of neurons in which, fol- lowing a period of strong hyperpolarization below the rest- ing membrane potential, the membrane potential briefly rebounds to a more depolarized level resulting in firing spikes. Rebound spiking is thus triggered by inhibition and not by direct sensory activation. After-discharges may also be evoked by rebounds through inhibitory networks (Macknik & Martinez-Conde, 2004; Macknik & Livingstone, 1998). Here we prefer to use the term rebound spikes 1 University of Barcelona, 2 Institute for Brain, Cognition, and Behavior, 3 Catalan Institution for Research & Advanced Stud- ies (ICREA) © 2010 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 23:2, pp. 491–501 Downloaded from http://direct.mit.edu/jocn/article-pdf/23/2/491/1774688/jocn.2010.21512.pdf by guest on 24 March 2021