Category-Specific Organization in the Human Brain Does Not Require Visual Experience

Abstract

Summary The ventral stream refers to a neural pathway that projects from early visual areas through to anterior temporal cortex, and comprises regions in ventral and lateral occipital-temporal cortex. The ventral stream is critical for recognizing visually presented objects. Functional imaging studies of the human brain have shown that different regions within the ventral stream show differential activation to nonliving (tools, houses) and living stimuli (animals, faces). The causes of these category preferences are widely debated. Using functional magnetic resonance imaging, we find that the same regions of the ventral stream that show category preferences for nonliving stimuli and animals in sighted adults, show the same category preferences in adults who are blind since birth. Both blind and sighted participants had larger blood oxygen-level dependent (BOLD) responses in the medial fusiform gyrus for nonliving stimuli compared to animal stimuli, and differential BOLD responses in lateral occipital cortex for animal stimuli compared to nonliving stimuli. These findings demonstrate that the medial-to-lateral bias by conceptual domain in the ventral stream does not require visual experience in order to develop, and suggest the operation of innately determined domain-specific constraints on the organization of object knowledge.

Connectivity-based constraints on category-specificity in the ventral object processing pathway

“…The idea that dimensions of organization that have nothing to do with category per se interact with statistical regularities in experience has recently gained momentum (e.g., Baker et al, 2007; Srihasam et al, 2014). One difficulty faced by proposals that assume a critical role for visual experience in driving category-specificity is that the broad organization by semantic domain in the ventral stream is present even in individuals with no visual experience (Striem-Amit et al, 2012; Mahon et al, 2009; Buchel et al, 1998; He et al, 2013). …”

“…Tools and other manipulable objects are an ‘eccentric’ class of things in the world for which both surface texture information (relevant for grasping) and action information (relevant for functional use) must be brought into register with visual form. For that reason, the underlying neural code in that region relates tool-specificity to connectivity to parietal action systems (Mahon et al, 2007; for evidence and discussion, see Almeida et al, 2013; Chen and Rogers, 2014; Gallivan et al, 2013; Hutchison et al, 2014; Mahon et al, 2009; 2013; Osher et al, 2015; Stevens et al, 2015). …”

“…Largely on the basis of neuropsychological data indicating there can be a widespread collapse of knowledge pertaining to a given category of items (for review see Mahon and Caramazza, 2009; 2011), as well as the fact that category-specificity does not depend on visual experience, we and others proposed that the basic scaffolding by semantic category derives from intrinsic (i.e., innate) patterns of structural connectivity between the ventral stream and regions outside of the ventral stream (Mahon et al, 2007; 2009; Mahon and Caramazza, 2011; Martin, 2006). More recently, Kanwisher and colleagues (Saygin et al, 2016; Osher et al, 2015) have presented compelling evidence that there is a high degree of topographical alignment between patterns of structural connectivity and patterns of category preferences.…”

“…For instance, both task-based (Pessoa et al 2006; Almeida et al 2013; Mahon et al 2013; Garcea & Mahon 2014) and resting functional connectivity (Zhang et al, 2009; Turk-Browne et al, 2010; Zhu et al, 2011; Simmons & Martin, 2012; Baldassano et al, 2013; He et al, 2013; Hutchison et al, 2014; O’Neil et al, 2014; Stevens, et al, 2015; Wang et al, 2015), as well as structural connectivity (Saygin et al, 2011; 2016; Mars et al, 2012; Bouhali et al, 2014; Osher et al, 2015), suggest alignment between stimulus preferences and connectivity to regions outside the ventral stream (for discussion of a connectivity-constrained account of category specificity, see Riesenhuber 2007; Martin, 2006; 2009; Mahon & Caramazza 2011; Chen & Rogers 2014; Behrmann & Plaut 2013; Mahon et al, 2007; 2009; Mahon, 2015). …”

Do you hear what I see?

“…A variety of studies have provided evidence for functional constancy in blind individuals. These showed that the visual-motion area of the brain responds to auditory and tactile motion 4, 5, 6 , that sounds made by objects are represented in brain regions associated with visual-object recognition 7, 8 , and that reading Braille elicits brain responses in the visual word-form area 9 .…”