Zaizhu Han

White matter structural connectivity underlying semantic processing: Evidence from brain damaged patients

Widely distributed brain regions in temporal, parietal and frontal cortex have been found to be involved in semantic processing, but the anatomical connections supporting the semantic system are not well understood. In a group of 76 right-handed brain-damaged patients, we tested the relationship between the integrity of major white matter tracts and the presence of semantic deficits. The integrity of white matter tracts was measured by percentage of lesion voxels obtained in structural imaging and mean fractional anisotropy values obtained in diffusion tensor imaging. Semantic deficits were assessed by jointly considering the performance on three semantic tasks that vary in the modalities of input (visual and auditory stimuli) and output (oral naming and associative judgement). We found that the lesion volume and fractional anisotropy value of the left inferior fronto-occipital fasciculus, left anterior thalamic radiation, and left uncinate fasciculus significantly correlated with severity of impairment in all three semantic tasks. These associations remained significant even when we controlled for a wide range of potential confounding variables, including overall cognitive state, whole lesion volume, or type of brain damage. The effects of these three white matter tracts could not be explained by potential involvement of relevant grey matter, and were (relatively) specific to object semantic processing, as no correlation with performance on non-object semantic control tasks (oral repetition and number processing tasks) was observed. These results underscore the causal role of left inferior fronto-occipital fasciculus, left anterior thalamic radiation, and left uncinate fasciculus in semantic processing, providing direct evidence for (part of) the anatomical skeleton of the semantic network.

Selectivity for large nonmanipulable objects in scene-selective visual cortex does not require visual experience

The principles that determine the organization of object representations in ventral temporal cortex (VTC) remain elusive. Here, we focus on the parahippocampal place area (PPA), a region in medial VTC that has been shown to respond selectively to pictures of scenes. Recent studies further observed that this region also shows a preference for large nonmanipulable objects relative to other objects, which might reflect the suitability of large objects for navigation. The mechanisms underlying this selectivity remain poorly understood. We examined the extent to which PPA selectivity requires visual experience. Fourteen congenitally blind and matched sighted participants were tested on an auditory size judgment experiment involving large nonmanipulable objects, small objects (tools), and animals. Sighted participants additionally participated in a picture-viewing experiment. Replicating previous work, we found that the PPA responded selectively to large nonmanipulable objects, relative to tools and animals, in the sighted group viewing pictures. Importantly, this selectivity was also observed in the auditory experiment in both sighted and congenitally blind groups. In both groups, selectivity for large nonmanipulable objects was additionally observed in the retrosplenial complex (RSC) and the transverse occipital sulcus (TOS), regions previously implicated in scene perception and navigation. Finally, in both groups the PPA showed resting-state functional connectivity with TOS and RSC. These results provide new evidence that large object selectivity in PPA, and the intrinsic connectivity between PPA and other navigation-relevant regions, do not require visual experience. More generally, they show that the organization of object representations in VTC can develop, at least partly, without visual experience.

The role of the left anterior temporal lobe in language processing revisited: Evidence from an individual with ATL resection

Various hypotheses about the role of the anterior temporal lobe (ATL) in language processing have been proposed. One hypothesis is that it binds the semantic/conceptual properties of words, functioning as a hub for linking modality-specific conceptual properties of objects. This hypothesis predicts that damage to ATL would give rise to impaired conceptual knowledge of all categories. A related school of hypotheses assumes that the left ATL is critical for lexical retrieval, with different sub-regions potentially important for different categories of items. We examined these hypotheses by studying a case of surgical resection of left ATL due to a low-grade glioma (LGG). Thorough language assessments performed four months after the operation revealed the following profile: the patient showed intact conceptual knowledge for all categories of items tested using both accuracy and response latency measures; he suffered from name retrieval deficits for proper names (people and place names) and artifacts (including tools), but showed no name retrieval difficulties for animate things. This pattern of results challenges both target hypotheses about the role of ATL in language processing tested here.

The Interaction between Semantic and the Nonsemantic Systems in Reading: Evidence from Chinese.

We report a Chinese-speaking patient WJX with left temporal lobe ischemic damage resulting in dementia. Similar to English speaking patients with this pathology, WJX showed impaired semantic system functioning together with a well preserved ability to read aloud Chinese characters including characters with unpredictable mappings between orthography and phonology-so called irregular characters. The summation hypothesis [Hillis, A. E., & Caramazza, A. (1991). Mechanisms for accessing lexical representations for output-evidence from a category-specific semantic deficit. Brain and Language, 40, 106-144; Hillis, A. E., & Caramazza, A. (1995). Converging evidence for the interaction of semantic and sublexical phonological information in accessing lexical representations for spoken output. Cognitive Neuropsychology, 12, 187-227] proposes that the good reading performance can be explained by the integration of a semantic route of reading and a nonsemantic route. Most Chinese characters contain components that can give a clue to the pronunciation (phonetic radical) and the meaning (semantic radical) of the character. We compared his comprehension and oral reading performance by varying the consistency of phonetic radicals and the transparency of semantic radicals. We observed an interaction between WJXs character comprehension and the consistency of the phonetic radical on reading performance; however, the transparency of semantic radicals had no effect on performance. We argue that this case report provides converging evidence for the principles of the summation hypothesis for reading.

Distinct Regions of Right Temporal Cortex Are Associated with Biological and Human–Agent Motion: Functional Magnetic Resonance Imaging and Neuropsychological Evidence

In human lateral temporal cortex, some regions show specific sensitivity to human motion. Here we examine whether such effects reflect a general biological–nonbiological organizational principle or a process specific to human–agent processing by comparing processing of human, animal, and tool motion in a functional magnetic resonance imaging (fMRI) experiment with healthy participants and a voxel-based lesion-symptom mapping (VLSM) study of patients with brain damage (77 stroke patients). The fMRI experiment revealed that in the lateral temporal cortex, the posterior superior temporal sulcus shows a preference for human and animal motion, whereas the middle part of the right superior temporal sulcus/gyrus (mSTS/STG) shows a preference for human and functional tool motion. VLSM analyses also revealed that damage to this right mSTS/STG region led to more severe impairment in the recognition of human and functional tool motion relative to animal motion, indicating the causal role of this brain area in human–agent motion processing. The findings for the right mSTS/STG cannot be reduced to a preference for articulated motion or processing of social variables since neither factor is involved in functional tool motion recognition. We conclude that a unidimensional biological–nonbiological distinction cannot fully explain the visual motion effects in lateral temporal cortex. Instead, the results suggest the existence of distinct components in right posterior temporal cortex and mSTS/STG that are associated, respectively, with biological motion and human–agent motion processing.

Intrinsic functional network architecture of human semantic processing: Modules and hubs

Semantic processing entails the activation of widely distributed brain areas across the temporal, parietal, and frontal lobes. To understand the functional structure of this semantic system, we examined its intrinsic functional connectivity pattern using a database of 146 participants. Focusing on areas consistently activated during semantic processing generated from a meta-analysis of 120 neuroimaging studies (Binder et al., 2009), we found that these regions were organized into three stable modules corresponding to the default mode network (Module DMN), the left perisylvian network (Module PSN), and the left frontoparietal network (Module FPN). These three dissociable modules were integrated by multiple connector hubs-the left angular gyrus (AG) and the left superior/middle frontal gyrus linking all three modules, the left anterior temporal lobe linking Modules DMN and PSN, the left posterior portion of dorsal intraparietal sulcus (IPS) linking Modules DMN and FPN, and the left posterior middle temporal gyrus (MTG) linking Modules PSN and FPN. Provincial hubs, which converge local information within each system, were also identified: the bilateral posterior cingulate cortices/precuneus, the bilateral border area of the posterior AG and the superior lateral occipital gyrus for Module DMN; the left supramarginal gyrus, the middle part of the left MTG and the left orbital inferior frontal gyrus (IFG) for Module FPN; and the left triangular IFG and the left IPS for Module FPN. A neuro-functional model for semantic processing was derived based on these findings, incorporating the interactions of memory, language, and control.

Nouns, verbs, objects, actions, and the animate/ inanimate effect

We report an aphasic patient, Z.B.L., who showed a significant advantage for verbs compared to nouns in picture-naming tests. Within the object class, he performed better on animate things than on nonliving things in picture naming as well as in an “attribute judgement task”. This pattern of performance is contrary to the central prediction of a recent proposal (Bird, Howard, & Franklin, 2000), which attributes noun–verb dissociation in aphasic patients to deficits in processing certain kinds of semantic features. This model proposes that conceptual representations of verbs have a lower proportion of sensory features than do representations of nouns; the same is proposed for inanimate versus animate items within the noun category. Noun deficits are assumed to arise due to impairment for the processing of sensory features. The model predicts that if a patient is more impaired for nouns than for verbs, he will also display more difficulty with animate than with inanimate objects. Contrary to predications derived from this theory, Z.B.L. performed better with animate than inanimate nouns.

The orthographic buffer in writing Chinese characters: Evidence from a dysgraphic patient

We investigated the postlexical processes in writing Chinese characters by studying the delayed copying performance of a Chinese dysgraphic patient, W.L.Z. His delayed copying difficulty could not be attributed to peripheral motor deficit and could not be readily explained by lexical or semantic factors. Instead, the copying performance was sensitive to a word length variable (number of logographemes), and the most prevalent errors were logographeme substitutions. Furthermore, in the substitution errors, the target logographemes and responses tended to share visual/motoric attributes. We propose that the delayed copying difficulty reflects a deficit to the buffering component in writing (coined “logographeme output buffer”), and the universality and language-specific features of the output buffer in writing are discussed.

How Visual Is the Visual Cortex? Comparing Connectional and Functional Fingerprints between Congenitally Blind and Sighted Individuals.

Classical animal visual deprivation studies and human neuroimaging studies have shown that visual experience plays a critical role in shaping the functionality and connectivity of the visual cortex. Interestingly, recent studies have additionally reported circumscribed regions in the visual cortex in which functional selectivity was remarkably similar in individuals with and without visual experience. Here, by directly comparing resting-state and task-based fMRI data in congenitally blind and sighted human subjects, we obtained large-scale continuous maps of the degree to which connectional and functional “fingerprints” of ventral visual cortex depend on visual experience. We found a close agreement between connectional and functional maps, pointing to a strong interdependence of connectivity and function. Visual experience (or the absence thereof) had a pronounced effect on the resting-state connectivity and functional response profile of occipital cortex and the posterior lateral fusiform gyrus. By contrast, connectional and functional fingerprints in the anterior medial and posterior lateral parts of the ventral visual cortex were statistically indistinguishable between blind and sighted individuals. These results provide a large-scale mapping of the influence of visual experience on the development of both functional and connectivity properties of visual cortex, which serves as a basis for the formulation of new hypotheses regarding the functionality and plasticity of specific subregions. SIGNIFICANCE STATEMENT How is the functionality and connectivity of the visual cortex shaped by visual experience? By directly comparing resting-state and task-based fMRI data in congenitally blind and sighted subjects, we obtained large-scale continuous maps of the degree to which connectional and functional “fingerprints” of ventral visual cortex depend on visual experience. In addition to revealing regions that are strongly dependent on visual experience (early visual cortex and posterior fusiform gyrus), our results showed regions in which connectional and functional patterns are highly similar in blind and sighted individuals (anterior medial and posterior lateral ventral occipital temporal cortex). These results serve as a basis for the formulation of new hypotheses regarding the functionality and plasticity of specific subregions of the visual cortex.

Cross-Modal Plasticity Preserves Functional Specialization in Posterior Parietal Cortex

In congenitally blind individuals, many regions of the brain that are typically heavily involved in visual processing are recruited for a variety of nonvisual sensory and cognitive tasks (Rauschecker 1995; Pascual-Leone et al. 2005). This phenomenon-cross-modal plasticity-has been widely documented, but the principles that determine where and how cross-modal changes occur remain poorly understood (Bavelier and Neville 2002). Here, we evaluate the hypothesis that cross-modal plasticity respects the type of computations performed by a region, even as it changes the modality of the inputs over which they are carried out (Pascual-Leone and Hamilton 2001). We compared the fMRI signal in sighted and congenitally blind participants during proprioceptively guided reaching. We show that parietooccipital reach-related regions retain their functional role-encoding of the spatial position of the reach target-even as the dominant modality in this region changes from visual to nonvisual inputs. This suggests that the computational role of a region, independently of the processing modality, codetermines its potential cross-modal recruitment. Our findings demonstrate that preservation of functional properties can serve as a guiding principle for cross-modal plasticity even in visuomotor cortical regions, i.e. beyond the early visual cortex and other traditional visual areas.