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

Abstract

Recent efforts to characterize visual object representations in the ventral object processing pathway in the human brain have led to contrasting proposals about the causes of neural specificity for different categories. Here we use multivariate techniques in a novel way to relate patterns of functional connectivity to patterns of stimulus preferences. Stimulus preferences were measured throughout the ventral stream to tools, animals, faces and places; separately, we measured the strength of functional connectivity of each voxel in the ventral stream to category-preferring regions outside the ventral stream. Multivariate analyses were then performed over ventral stream voxels, relating ‘category-preferences’ to ‘functional connectivity preferences’. We show that the relation of those two measures doubly dissociates ‘tools’ and ‘places’, within what is ostensibly ‘place’ selective cortex (parahippocampal gyrus). Specifically, in the parahippocampal gyrus, functional connectivity to the left inferior parietal lobule is selectively related to stimulus preferences for tools (and not places), while functional connectivity to retrosplenial cortex is selectively related to place preferences (and not tools preferences). These findings indicate that functional connectivity can be used to index representational content rather than just provide an understanding of ‘which regions are talking to which regions’. We suggest that the connectivity of the brain is what drives category-specificity in the ventral stream, and that if this is correct, then understanding the connectivity of the ventral stream will be key to understanding the causes and function of category-specific neural organization.

Structural Disconnection of the Tool Use Network After Left Hemisphere Stroke Predicts Limb Apraxia Severity

“…Voxels in lateral occipitotemporal cortex respond to images of hands (Orlov et al, 2010) and tools (Bracci et al, 2012), and exhibit functional connectivity to the left inferior parietal lobule (Bracci et al, 2012;Mahon et al, 2007). Furthermore, parietal disconnection extended to ventral temporal cortex to include the fusiform gyrus, consistent with prior functional connectivity findings in apraxia (Watson et al, 2019) and in neurotypical adults (Garcea & Mahon, 2014; see also Chen et al, 2017;Stevens et al, 2015). In light of these findings, it has been argued that the processing of object properties in ventral temporal cortex provides an input to the praxis system, because the extraction of visual attributes of objects (e.g., whether an object is slippery, hot, or sharp) as well as stored knowledge of material properties (e.g., object weight; Gallivan et al, 2014) informs the retrieval of hand posture and deployment of an object-directed grasp when functionally manipulating a tool for discussion, see Gallivan & Culham, 2015).…”

Gesturing tool use and tool transport actions modulates inferior parietal functional connectivity with the dorsal and ventral object processing pathways

“…A number of fMRI studies have demonstrated there is a high degree of cross-talk between the dorsal and ventral visual pathways as a function of grasping or generating tool-directed gestures (e.g., see Budisavljevic, Dell'Acqua, & Castiello, 2018;Garcea et al, 2018;Hutchison & Gallivan, 2018) or when viewing objects or making judgments about object manipulation (e.g., Chen, Snow, Culham, & Goodale, 2018;Chen et al, 2017;Freud, Rosenthal, Ganel, & Avidan, 2015;Kleineberg et al, 2018;Sim, Helbig, Graf, & Kiefer, 2015; for discussion, see Orban & Caruana, 2014;van Polanen & Davare, 2015). Our results offer a novel interpretation of the role that the left SMG plays in tool-directed actions: Tool manipulation knowledge is not "represented" in the left SMG; rather the left SMG sits at the nexus of the dorso-dorsal and ventro-dorsal visual pathways, and serves as an intermediary or "hub" region aggregating (a) representations of object properties and conceptual knowledge in the ventral stream with (b) online sensory-motor information processed in the dorsal stream, (c) which is informed by top-down biasing signals from prefrontal cortex to resolve competition between candidate tool use actions.…”

“…Prior to the scan, careful training and instruction was given to participants to pantomime tool use and tool transport actions. The training procedure was identical to previous training instructions we have administered to participants (e.g., Chen et al, , ; Chen, Garcea, et al, ; Erdogan, Chen, Garcea, Mahon, & Jacobs, ; Garcea et al, ) in which participants are trained to generate a gesture as if the tool stimulus was “in‐hand.” Importantly, because participants are in a physically constrained environment in the bore of the magnet, they were instructed to generate gestures at a slow rate (∼1 gesture per second) for the duration of the event; because there was no visual feedback during scanning (i.e., each participant's right hand was out of sight during the scan), the experimenter ensured that the participants memorized the tool transport and tool use actions prior to the scan by asking them to generate each action from memory. During each run the experimenter visually inspected the participant's gesturing action in real time to verify that the participants were generating actions when cued by the experiment.…”

Spontaneously emerging patterns in human visual cortex and their functional connectivity are linked to the patterns evoked by visual stimuli

“…Recent work has also shown that voxel-wise resting FC in visual cortex is better approximated by the FC evoked by movies than by more artificial stimuli such as rotating checkerboards or static pictures of stimuli (Strappini et al 2018, Wilf et al 2017. Finally, Chen and colleagues (Chen et al 2017) measured the voxelwise resting FC between regions of ventral visual cortex and a second region that was functionally related to a specific visual category (e.g. tools).…”

“…This analysis bears some resemblance to a representational similarity analysis, which is a standard methodology for identifying the representational content of evoked activity in a brain region (Kriegeskorte et al 2008). Unlike Chen et al (Chen et al 2017), we examine the multi-vertex pattern of resting activity at each timepoint rather than separately analyzing each individual vertex over timepoints in a resting FC analysis.…”