Domain-specific connectivity drives the organization of object knowledge in the brain

Abstract

The goal of this chapter is to review neuropsychological and functional MRI findings that inform a theory of the causes of functional specialization for semantic categories within occipito-temporal cortex-the ventral visual processing pathway. The occipito-temporal pathway supports visual object processing and recognition. The theoretical framework that drives this review considers visual object recognition through the lens of how "downstream" systems interact with the outputs of visual recognition processes. Those downstream processes include conceptual interpretation, grasping and object use, navigating and orienting in an environment, physical reasoning about the world, and inferring future actions and the inner mental states of agents. The core argument of this chapter is that innately constrained connectivity between occipito-temporal areas and other regions of the brain is the basis for the emergence of neural specificity for a limited number of semantic domains in the brain.

Keywords: Category-specificity; Concepts; Domain-specificity; Neural specificity; Objects; Occipito-temporal cortex; Ventral visual pathway.

Figure 1.. A domain-specific network for physical reasoning about how first person actions will change the state of the world (aka, the ‘tool processing network’).

The maps show functional MRI data obtained while participants viewed and named images of common tools (fork, cup) compared to images of animals and faces. All of the regions, with the exception of LO, are defined as expressing differential neural (BOLD) responses for images of ‘tools’ compared to the baseline category of ‘animals.’ LO was defined by the contract of all intact stimuli (tools, animals, places, face) compared to phase-scrambled images. Regions are color-coded based on the principal dissociations that have been documented in the neuropsychological literature (Panel B). The first functional MRI studies describing this set of “tool-preferring” regions were carried out in the laboratory of Alex Martin (L. Chao et al., 1999; Chao & Martin, 2000). B. For each process/function depicted by a ‘box’, there are neuropsychological studies indicating that process can be separately impaired in individuals with acquired brain injury. The schematic depicts a hypothesized series of dependencies among those dissociable processes in support of an account of ‘functional’ object grasping (e.g., end-state comfort). Figure reproduced from (B. Mahon, 2020). The network of regions shown in Panel A has been described as the ‘Tool Processing Network’ (FE Garcea & Mahon, 2014). Calling that network the ‘tool-processing network’ is descriptive of the types of stimuli that engage those regions. By hypothesis, the broader computational goal of the network shown in Panel A is physical reasoning about how first person actions will change the state of the world (B. Mahon, 2020). On this analysis, functional object use is much broader than tool processing per se: ‘Tools’, or manipulable objects more generally, are a class of things in the world for which successful processes requires the specific processes represented across the network.

Figure 2.. Category-specific semantic deficits.

A. Patients with category-specific semantic deficits may have selective impairments for naming items from one category of items compared to other categories. B. Those patients may also have impairments for answering questions about all types of object properties (i.e., visual/perceptual and functional/associative) pertaining to the impaired category (for references and discussion, see (Caramazza & Mahon, 2003), from which the figure was reproduced).

Figure 3.. Alignment of category-preferences in the ventral stream with functional connectivity to category-preferring regions outside of the ventral stream.

A. Category-preferring regions outside ventral occipito-temporal cortex were defined for animals (Superior temporal sulcus), places (retrosplenial cortex), and tools (parietal cortex). B. Whole-brain functional connectivity maps were generated over resting fMRI data using each of the Regions of Interest (ROIs) outside of ventral occipito-temporal cortex as a seed (the figure shows the results only for ventral temporo-occipital cortex). C. Separately, category-preferences for animals, places, and tools were computed in the ventral stream. D. Linear correlation was used over ventral stream ROIs to relate the multi-voxel pattern of functional connectivity (to regions outside the ventral stream) to category-preferences. E. In medial ventral ROIs (place and tool preferring areas), the multivoxel pattern of functional connectivity to retrosplenial cortex was related to place preferences but not tool preferences, shown in the blue bars; over the same pool of medial ventral stream voxels, the multivoxel pattern of functional connectivity to parietal cortex was related to tool preferences but not place preferences, shown in the green bars. F. In lateral ventral ROIs, the multivoxel pattern of functional connectivity to the superior temporal sulcus was related to animal (and face, not shown) preferences (red bars), but not to tool or place preferences.

Figure 4.. Causal evidence that neural responses to manipulable objects in occipito-temporal cortex depend on real-time processing in parietal cortex.

Two recent findings provide causal evidence for the hypothesis that processing of manipulable objects in the ventral stream is modulated by parietal action representations. Garcea and colleagues (F. E. Garcea et al., 2019) found that lesions involving aIPS were associated with reduced fMRI responses to tool stimuli in medial ventral temporal areas; however, lesions to aIPS were not associated with reduced responses to place stimuli in the same regions (Panel A). This is despite the fact that, if anything, neural responses in medial ventral occipito-temporal areas stronger for place than tool stimuli. A whole-brain analysis that searched for where BOLD activity was inversely related to the probability of a lesion to aIPS, identified the medial fusiform gyrus and collateral sulcus (Panel B; this analysis also identified the posterior inferior/middle temporal gyrus). In a separate study, in healthy participants, Lee and colleagues (Lee et al., 2019) found that cathodal tDCS to left parietal cortex disrupted voxel-wise pattern discriminability between tools and animals (Panel C) in medial ventral occipito-temporal cortex, but not in lateral aspects of the fusiform gyrus (face preferring area). Neural similarity among tool stimuli was increased after excitatory (anodal) stimulation of left parietal cortex and reduced after inhibitory (cathodal) stimulation of left parietal cortex. Moreover, as shown in Panel D, cathodal versus anodal stimulation modulated effective functional connectivity between SMG and the medial fusiform gyrus for tool, but not for place stimuli. These findings indicate that parietal representations of object-directed action causally modulate, online, visual object processing of graspable objects in occipital-temporal cortex.