Elsevier

Neuropsychologia

Volume 84, April 2016, Pages 244-251
Neuropsychologia

Cognitive and anatomic double dissociation in the representation of concrete and abstract words in semantic variant and behavioral variant frontotemporal degeneration

https://doi.org/10.1016/j.neuropsychologia.2016.02.025Get rights and content

Highlights

  • The anatomical representations of abstract and concrete concepts are investigated.

  • Tested two patient groups, svPPA and bvFTD, with atrophy to theoretically critical neural regions.

  • A two-alternative forced choice task was administered, using concrete and abstract noun stimuli.

  • svPPA patients had worse concrete word knowledge, related to the left inferior temporal gyrus.

  • bvFTD patients had worse abstract word processing, related to the inferior frontal gyrus.

Abstract

We examine the anatomic basis for abstract and concrete lexical representations in semantic memory by assessing patients with focal neurodegenerative disease. Prior evidence from healthy adult studies suggests that there may be an anatomical dissociation between abstract and concrete representations: abstract words more strongly activate the left inferior frontal gyrus relative to concrete words, while concrete words more strongly activate left anterior-inferior temporal regions. However, this double dissociation has not been directly examined. We test this dissociation in two patient groups with focal cortical atrophy in each of these regions, the behavioral variant of Frontotemporal Degeneration (bvFTD) and the semantic variant of Primary Progressive Aphasia (svPPA). We administered an associativity judgment task for abstract and concrete words, where subjects select which of two words is best associated with a given target word. Both bvFTD and svPPA patients were significantly impaired in their overall performance compared to controls. While controls treated concrete and abstract words equally, we found a category-specific double dissociation in patients’ judgments: bvFTD patients showed a concreteness effect (CE), with significantly worse performance for abstract compared to concrete words, while svPPA patients showed reversal of the CE, with significantly worse performance for concrete over abstract words. Regression analyses also revealed an anatomic double dissociation: The CE is associated with inferior frontal atrophy in bvFTD, while reversal of the CE is associated with left anterior-inferior temporal atrophy in svPPA. These results support a cognitive and anatomic model of semantic memory organization where abstract and concrete representations are supported by dissociable neuroanatomic substrates.

Introduction

Central to the question of how semantic concepts are organized in the brain is the debate of whether abstract and concrete word categories have distinct representations. While concrete words have referents with sensory-motor features, abstract words refer to concepts that primarily exist within the mind and via language (Hale, 1988). However, it is uncertain if this concrete-abstract distinction has a basis in the neuroanatomic representation of these categories.

Two historically dominant theories of concrete and abstract word representation are the dual-coding theory and the context availability hypothesis. The dual-coding theory proposes that, while both abstract and concrete words have linguistically-based representations, only concrete words have additional visually-based representations that draw from their physical referents (Paivio, 1989, ). Indeed, concrete words tend to have more predicate features associated with them than abstract words, and these features facilitate word knowledge and recognition (Recchia and Jones, 2012; Hill et al., 2014). The richness of concrete feature representations offers an explanation for the concreteness effect (CE)-the tendency for individuals to be more accurate and faster when identifying concrete words compared to abstract words. The dual-coding view is closely aligned with more current theories of semantic memory related to grounded cognition. These theories propose that sensory-motor features in part underlie conceptual knowledge, and that neural systems associated with sensory-motor processing help support lexical processing (Barsalou, 2008, Binder and Desai, 2011). Thus, the representations of both abstract and concrete concepts are hypothesized to be supported by language regions in the perisylvian areas of the left hemisphere. However, only concrete word processing receives additional support from the inferior temporal cortex and surrounding regions associated with high level visual processing and the representation of visual-perceptual and object feature knowledge (, , , ). In support of these perspectives, evidence from functional imaging studies show that recognition of concrete words activates extensive areas associated with visual feature and object processing, including the inferior temporal cortices, and the fusiform and parahippocampal gyri (Mellet et al., 1998; , ).

An alternative view is the context availability hypothesis, which posits that word knowledge and recognition depend in part on the associated context (Schwanenflugel et al., 1988). Because concrete referents have physical or temporal existence, these words appear in a more consistent and relatively narrow set of contexts. In comparison, abstract words tend to be more semantically diverse than concrete words, appearing in a larger variety of contexts, and with more variations in their meaning. For example, the general meaning of the word “honor” is high respect or reputation, but the specific meaning can change depending on context: “honor” can refer to a privilege, as in “it is my honor”; an achievement, as in “graduated with honors”; or a title, as in “your Honor, I object”. The need to select from different possible interpretations may explain why abstract words can take longer to identify than concrete words, especially when context is minimal. Moreover, relevant context has been shown to facilitate the recognition of abstract words, so that they are processed as quickly as concrete words (Schwanenflugel and Shoben, 1983; van Hell and De Groot, 1998). Similarly, abstract word comprehension, more than concrete, is supported by accessing closely semantically associated words (, ). Because of this reliance on context, abstract words may partially depend on executive functioning and semantic control to regulate meaning selection. In support of this view, imaging studies in healthy adults demonstrate that the processing of abstract words activates the inferior frontal gyrus (, ), an area thought to be involved in semantic control (, ) and in the integration of contextual information (Hoffman et al., 2015).

Here we investigate the cognitive and anatomical representation of abstract and concrete words, and evaluate our results in the context of grounded cognition and context availability theories. To assess semantic memory, subjects participated in a two-alternative forced-choice task, where they were asked to select which of two nouns best associates with a target noun; half of trials were composed of abstract nouns, and half were concrete. We examine semantic processing in two patient groups with atrophy to regions implicated in object feature processing and in semantic control: patients with semantic variant primary progressive aphasia (svPPA) and with behavioral variant frontotemporal degeneration (bvFTD), respectively. We test concrete word knowledge in svPPA, a form of primary progressive aphasia characterized by impaired confrontation naming and poor word comprehension (Hodges and Patterson, 2007; Mesulam et al., 2003). This patient group presents with profound atrophy to the anterior inferior temporal cortex (Amici et al., 2007, , , , ). Poor concrete knowledge in svPPA has been previously observed, with several studies showing a reversal of the CE-selectively worse concrete word knowledge and recognition, compared to abstract (, , , , ). While this is not seen in all studies (, ), differences in impairment are possibly due to variability in the location and progression of atrophy in svPPA (, ). We directly assess the relationship between relative difficulty with concrete word knowledge and atrophy to the inferior temporal gyrus in svPPA. We also compare svPPA performance to that of bvFTD patients, a social disorder typified by social disinhibition, apathy, and personality changes. Importantly, these patients present with impaired executive functioning along with frontal lobe atrophy (Rascovsky et al., 2011). While bvFTD is not typically associated with impaired semantic knowledge, this may be due in part to the design of standard semantic memory assessments, whose stimuli largely consist of concrete words (e.g. Boston Naming Test, Kaplan et al., 2001; and Pyramids and Palm Trees Test, Howard and Patterson, 1992). If executive functioning and semantic control processes are important for abstract meaning selection, we expect impaired processing for abstract words to be found in bvFTD, and we expect this to relate to atrophy of the inferior frontal gyrus in these patients.

Section snippets

Subjects

Participants were 12 right-handed, English speakers that were diagnosed with svPPA and 18 patients diagnosed with bvFTD, based on the consensus diagnostic criteria outlined by Gorno-Tempini et al. (2011) and Rascovsky et al. (2011), respectively. We compared the performance of these patients with 18 healthy older adult controls. Of the 12 svPPA patients, 10 also had co-occurring mild behavioral symptoms. Co-occurrence of behavioral symptoms with svPPA is typical, and is representative of the

3.1.1. Overall accuracy for Associativity task

Mean overall performance in the associativity task is shown in Fig. 1. A univariate ANOVA revealed a significant effect of patient group (svPPA, bvFTD, Control) on accuracy (F(2,45)=17.83, p<0.001). Compared to healthy controls, accuracy was significantly impaired for both svPPA (F(28)=56.27, p<0.001) and bvFTD (F(34)=22.40, p<0.001). Overall accuracy was not significantly different between svPPA and bvFTD patients.

3.1.2. Concrete vs. abstract accuracy

An ANOVA with a 2 (Condition: Abstract, Concrete) X 3 (Group: svPPA, bvFTD,

Discussion

This study revealed an anatomical double disassociation between abstract and concrete word representations by examining single word semantic deficits in svPPA and bvFTD. While controls showed equally accurate performance for concrete and abstract words, bvFTD patients demonstrated significantly worse performance for abstract words, and svPPA patients were significantly worse for concrete than abstract words, showing a reversal of the CE. We related this dissociation in performance to regions of

Conflicts of interest

The authors have no conflicts of interest to report.

Acknowledgement

This work was supported in part by NIH (AG017586, NS044266, AG038490, AG053488), the Wyncote Foundation and the Arking Family Foundation.

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