Preserved recognition of basic visual features despite lack of awareness of shape: Evidence from a case of neglect

The visual system is bombarded by an immense amount of information at every glance. Decades of research have revealed that dedicated networks extract and process information such as orientation, color, and motion of stimuli at every location in the visual field to create a coherent visual experience (Hubel & Wiesel, 1968; Livingstone & Hubel, 1988; Zeki et al., 1991). The visual system achieves this feat in part by segmenting and processing individual objects and processing their various properties in parallel (e.g., a mug, red, blue stripes). Spatial attention is thought to play a role in creating a coherent perceptual experience (a red mug with blue stripes) by integrating visual information coming from a given location (Humphreys et al., 2000; Kahneman et al., 1992; Robertson, 2003; Treisman & Gelade, 1980; Wolfe & Bennett, 1997; Wolfe & Horowitz, 2004). Despite this insight, the mechanisms underlying this integration process are not entirely understood.

One source of insight regarding the mechanisms of spatial attention in visual recognition comes from deficits of spatial attention, in which the integration of object features does not occur normally. In this study, we examined the perception of visual features (shape, color, and orientation) in an individual with hemispatial neglect, DH. Through study of his patterns of behavior, we gain insight into how visual features of objects are accessed and combined in visual object recognition, and the mechanisms of spatial attention in this process.

Hemispatial neglect is an acquired disorder of spatial attention, often resulting from damage to right hemisphere parietal and/or frontal cortices (Bisiach, 1993; De Renzi, 1982; Vallar & Perani, 1987). In the absence of sensory processing deficits, individuals with neglect typically lose awareness of visual information on the side of space opposite to their lesion, the contralesional side (Lunven & Bartolomeo, 2017; Vallar & Calzolari, 2018). For instance, an individual with a right hemisphere lesion might ignore the left side of an object (e.g., fail to notice and thus to eat food on the left side of their plate) or make errors in reading on the left side of a word (e.g., read dice as “race”).

The statement that neglect affects the left half of an object already implies that there must be sufficient processing of the entire object so that its boundaries and center can be defined by the visual system. Supporting this idea, individuals with neglect can segment images based on low-level visual information, including information present on the neglected side (Driver & Mattingley, 1998). For instance, in typical perception, symmetrical shapes stand out as figures while concurrently present asymmetrical shapes are perceived as background (Kanizsa & Gerbino, 1976). Despite individuals with neglect being unable to explicitly judge the symmetry of a figure due to a deficit in accessing left-sided information, they still exhibit a preference for symmetry in figure-ground segmentation (Driver et al., 1992). In summary, there is evidence that basic perceptual processes such as figure-ground segmentation can be carried out without awareness and this segmentation can influence task responses (for review of similar evidence in neurotypical subjects, Vandenbroucke et al., 2014).

In addition to implicit processing of spatial extent, individuals with neglect can also show implicit knowledge about the nature of stimuli or stimulus parts they fail to report, as documented with indirect measures such as priming. For instance, individuals with neglect might fail to detect an object on the left side of the visual field (e.g., a drawing of an apple), yet respond faster to a subsequently presented word if it is semantically related to the missed object (e.g., after apple, faster for tree compared to truck, see Audet et al., 1991; Berti & Rizzolatti, 1992; Kristjánsson et al., 2005). Thus, neglected stimuli can be processed implicitly to some extent and affect later processing of other objects.

Taken together, previous research into information processing in neglect has revealed a dissociation between the availability of implicit and explicit information about visual stimuli on the neglected side. The evidence for figure-ground segmentation and implicit encoding of stimulus properties on the left side shows that neglected visual properties can be unconsciously processed to a certain extent even when they are not consciously perceived. This pattern supports the long-held view that focused spatial attention is required for overt recognition of stimulus properties (Beck et al., 2001; Deouell, 2002; Driver & Mattingley, 1998; Driver & Vuilleumier, 2001; Rafal, 1994; Treccani et al., 2012; Van Vleet & Robertson, 2009; Vuilleumier et al., 2001).

In previous work, it was generally assumed that when an individual with neglect is unaware of visual information at a particular location, it reflects a failure to attend, preventing overt recognition of all information residing in that location. Despite the established understanding that visual information goes through the visual system through various channels, reflecting distinctions such as magnocellular and parvocellular systems or different visual features (Cowey, 1985; Grill-Spector et al., 1998; Hubel & Wiesel, 1962; Kaplan & Shapley, 1986; Kourtzi & Kanwisher, 2001; Zeki, 1993), the way attentional failures affect processing of different visual features has not been studied in much detail. There are some notable exceptions to this trend. For instance, Doricchi et al. (1996) demonstrated that some patients exhibit neglect symptoms specifically for low luminance contrast stimuli but not for those defined by high color contrast (Doricchi et al., 1996, 1997). There is also a case report of a painter with neglect who encountered more difficulty in incorporating color on the left side of his drawings while demonstrating better performance in drawing shape (Blanke et al., 2003). These demonstrations illustrate the in-principle separation of how spatial attention interacts with visual information via different visual channels. Still, it is generally understood that if a portion of a stimulus is neglected, none of its properties can be reported (Treccani et al., 2012; Treisman & Gelade, 1980; Van Vleet & Robertson, 2009).

In this study, we report a novel and complementary case of left-neglect, an individual we refer to as DH, who shows selective lack of awareness of left-side information about object shape while retaining the ability to report color defined within the same object's boundaries. Furthermore, he can also report the location and orientation of a colored region on the neglected left side despite lack of awareness of the shape of the region. To our knowledge, selective impairment for shape along with preserved recognition of other visual features in the same spatial location has not been reported in other cases of neglect. DH's behavioral profile thus raises questions regarding how visual features of objects are accessed in visual object recognition, and the role of spatial attention in this process.

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