Elsevier

Brain and Language

Volume 111, Issue 1, October 2009, Pages 8-19
Brain and Language

A common mechanism in verb and noun naming deficits in Alzheimer’s patients

https://doi.org/10.1016/j.bandl.2009.07.009Get rights and content

Abstract

We tested the ability of Alzheimer’s patients and elderly controls to name living and non-living nouns, and manner and instrument verbs. Patients’ error patterns and relative performance with different categories showed evidence of graceful degradation for both nouns and verbs, with particular domain-specific impairments for living nouns and instrument verbs. Our results support feature-based, semantic representations for nouns and verbs and support the role of inter-correlated features in noun impairment, and the role of noun knowledge in instrument verb impairment.

Introduction

Semantic impairments in Alzheimer’s disease (AD) have been central to several theoretical accounts of semantic memory, but much of the research on these impairments has focused on nouns (e.g., Bonilla and Johnson, 1995, Garrard et al., 2001, Gonnerman et al., 1997, Hodges and Patterson, 1995). Although nouns are an essential part of language, it is the lexical representation of verbs that is often considered most crucial for certain aspects of language processing, most notably sentence comprehension (e.g., Boland et al., 1990, MacDonald et al., 1994). Recently, several researchers have recognized the importance of verb semantic performance for the overall understanding of semantic impairments in AD and have begun to explore verb performance in these patients (e.g., Druks et al., 2006, Fung et al., 2001, Grossman et al., 1996, Grossman et al., 1997, Parris and Weekes, 2001, Robinson et al., 1996). Despite these efforts, the extent and nature of verb impairments in this population remains controversial. The research reported here aims to advance our understanding of the verb impairments in AD by establishing whether theoretical constructs and models that have been developed to account for noun and verb naming impairments can explain the performance of AD patients. In particular, we investigate the implications of naming deficits for the previously hypothesized organization of semantic representations of nouns and verbs within a feature-based framework.

The semantic representation of abstract nouns and verbs is not well understood even in unimpaired populations and we therefore chose to only examine impairments to imageable nouns and verbs. Although this choice may restrict the generality of our results, it allowed us to address the broader theoretical implications of our finding by relating it to previous theoretical work on the semantic representation of concrete nouns. In particular, we wanted to see whether AD patients’ verb impairment can be captured in the same feature-based distributed representation framework that several investigators have used to explain semantic deficits with concrete nouns (e.g., Aronoff et al., 2006, Devlin et al., 1998, Gonnerman et al., 1997, Saffran and Sholl, 1999, Shallice, 1993, Tyler and Moss, 2001). In a feature-based framework, conceptual knowledge is represented by connections between features and concepts, and the activation of concepts corresponds to a pattern of activation over distributed featural representations. In this framework, the relation between concepts is based on the number of features the two concepts share (featural overlap), which largely maps onto perceived similarity between concepts (Maki et al., 2006, Rips et al., 1973, Tversky, 1977). Featural overlap also gives rise to other relations beyond similarity. For instance, “contrast coordinate” relations exist between concepts that differ in only a small number of features (e.g., zebra and horse), and “super-ordinate” relations exist when the features of one concept are a subset of another concept’s features (e.g., animal and horse).

Although the majority of the work on the relationship between the structure and organization of the featural system and semantic performance has centered on concrete nouns (e.g., Cree and McRae, 2003, Garrard et al., 2001, McRae et al., 1997), some researchers have also investigated the role of features in verbs (e.g., Bird et al., 2000, Miller and Fellbaum, 1991, Parris and Weekes, 2001, Vigliocco et al., 2002, Vigliocco et al., 2004, Vinson and Vigliocco, 2002, Vinson et al., 2003). The present research extends this previous work in two ways. First, we examined whether the general feature-based framework can account for verb performance in AD by testing a main prediction of this framework – graceful degradation (i.e., the gradual loss of function). Second, we tested the predictions of several specific feature-based models by comparing patients’ performance with nouns and verbs from different semantic domains. We discuss each of these in turn.

A hallmark characteristic of the distributed feature-based framework is that it predicts graceful degradation, rather than complete dysfunction, as a result of small amounts of damage to the conceptual system. Graceful degradation occurs in this framework as a result of gradual loss of connections between features and the concepts which they represent, mirroring the likely neurodegenerative effect of AD (Farah & McClelland, 1991). With the progression of the disease, the number of available semantic features gradually decreases. As a result, differences between concepts diminish, even though the gross structure of semantic categories may remain largely intact initially (Aronoff et al., 2006). Thus, graceful degradation means that AD patients’ performance on semantic tasks looks similar to unimpaired performance, except that it’s poorer overall. The general preservation of semantic category structure at the initial stages of disease progression has been previously shown for nouns (Aronoff et al., 2006, Bonilla and Johnson, 1995, Ober and Shenaut, 1999), but no similar evidence currently exists for verbs. Because nouns and verbs differ in a variety of ways, their susceptibility to damage may be different. While concrete nouns tend to refer to individuated referents, verbs tend to describe relations (e.g., Gentner, 1981). Their semantic representations may be more dependent on the representations of other concepts, leading to faster breakdown of category structure. Moreover, because verb meaning is intimately connected to the syntactic structures the verb can appear in, verb impairments may appear all-of-a-piece with the decline of grammatical ability (Grossman et al., 1996, Kempler et al., 1998). However, if the same feature-based organizational principles underlie the semantic representations of nouns and verbs, then AD patients’ verb performance should also show graceful degradation in that patients should show greater difficulty with the same semantic categories that healthy controls find more difficult. The first goal of the present work was to test whether, similar to nouns, AD patients’ verb performance resembles unimpaired performance, albeit at an overall lower level.

Graceful degradation also predicts consistent changes to the pattern of errors made by patients as the disease progresses (e.g., Bowles et al., 1987, Gonnerman et al., 2004, Hodges et al., 1995). This process occurs in the following way: When all the connections between features and the concepts they represent are intact, accuracy is expected to be high. With mild damage to these connections, most knowledge will be preserved, but if a distinguishing feature is affected then contrast coordinate errors may occur (e.g., saying dog for cat). Increasing damage will affect more distinguishing features which will likely result in a substantial loss of knowledge about specific concepts, reflected in a high number of super-ordinate errors (e.g., saying animal for cat). More extensive damage will lead to the loss of even general knowledge about concepts, which will likely be reflected in the occurrence of cross-category errors (e.g., saying pear for cat). Finally, with massive damage to the connections in the featural system, loss of knowledge of entire semantic categories may occur, resulting in the complete loss of naming ability for concepts from these categories, and leading to many do not know responses. Although the general pattern of noun naming errors exhibited by patients appears to support this prediction (Bowles et al., 1987, Gonnerman et al., 2004, Hodges et al., 1995), it is yet unclear whether the same error progression would also occur with verbs. Verb performance may not exhibit the same pattern of errors, given the conceptual differences between nouns and verbs (Gentner, 1981) and their differing syntactic roles (Grossman et al., 1996). However, if the same feature-based organizational principles underlie the semantic representation of nouns and verbs then verb naming errors should show similar patterns to nouns. The second specific goal of the present work was to test this prediction.

So far, we focused on whether verb performance in AD, at least for imageable verbs, could be explained in a feature-based framework on the basis of general mechanisms that are similar to the ones previously used to explain noun performance. We now turn to address the question of whether verb performance in AD may in fact show that verbs and nouns are represented in a single feature-based system. The general feature-based approach does not necessarily entail shared representations for nouns and verbs, and different researchers working in this framework have taken different positions about this issue. For example, in research on general models of semantic memory, Miller and Fellbaum (1991) described a feature-based network model in which nouns and verbs are represented separately, but Vigliocco et al. (2004) modeled the semantic representation of objects and actions within a single unitary feature-based system.

In the context of semantic impairments, Bird et al. (2000) proposed a model of semantic impairments in which nouns and verbs are represented in a single unitary feature-based semantic system. Following Warrington and McCarthy, 1987, Warrington and Shallice, 1984 seminal work on nouns, Bird, Howard, and Franklin argued that verbs are similar to non-living nouns, in that they rely on a relatively low proportion of sensory to functional features. Their model predicts an association between performance with non-living nouns and verbs, which they confirmed by testing a small group of patients with aphasia. Parris and Weekes (2001) extended this approach to predict an association between performance with nouns and performance with instrument verbs, which encode a typical instrument as part of their core meaning (e.g., sweeping). In support of their model, Parris and Weekes described an anomic patient with dementia who showed worse performance with nouns than with verbs, but also a more subtle category specific verb deficit, with instrumental verbs being more impaired than non-instrumental verbs.

A plausible extension of this model is that, due to the importance of instrument information for the semantic representation of instrument verbs, coupled with the fact that those instruments tend to belong to non-living noun categories, semantic performance with instrument verbs would be associated with non-living noun performance more than with living nouns performance. Although Parris and Weekes (2001) acknowledged this implication of their model, the single patient that they tested was completely impaired with all nouns, and they were therefore unable to test this prediction directly. Here we tested this prediction of the Parris and Weekes model by comparing instrument verb performance and relative non-living and living noun performance in a group of AD patients with various levels of impairment. Following the same logic, we reasoned that performance with verbs that rely on sensory information would be associated with performance with nouns that describe living things more than with nouns that describe non-living things. We, therefore, also looked at manner verbs whose meaning encodes the manner of the action they describe (e.g., run, skip, and walk), which, by some accounts (Marshall et al., 1996, Marshall et al., 1996), is primarily sensory (e.g., 〈quick movement〉 is a perceptual/visual feature that distinguishes running from walking). Under this view, the Bird, Howard, and Franklin, and Parris and Weekes models should predict a stronger association between performance with manner verbs and living nouns.

In addition to the distinction between sensory and functional features, some researchers also consider the likelihood with which features co-occur in the representation of different concepts (feature inter-correlation; e.g., animals that 〈have a beak〉 tend to also 〈fly〉) as an important predictor of semantic impairments (Devlin et al., 1998, Grossman et al., 1997, Moss et al., 1997). Garrard et al., 2001, McRae et al., 1997 analyzed differences in the prevalence of inter-correlated features in different semantic noun categories and found that living noun categories had more inter-correlated features than non-living categories. Due to the differences in the number and type of inter-correlated features in different domains, several researchers have used feature inter-correlation to explain domain-specific deficits with nouns. Gonnerman et al. (1997) argued that the semantic representation of living things is protected from small amounts of damage by the high prevalence of feature inter-correlation. If one feature in an inter-correlated cluster is damaged, the rest of the features in the cluster can still lead to sufficient activation of the concept. In contrast, because non-living concepts tend to depend on idiosyncratic features, damage to one feature is more likely to impair performance with any non-living concept that relies on that feature. Moss et al. (1997) applied a similar logic but also differentiated between distinctive and shared features. They noted that distinctive features tend to appear in inter-correlated clusters more often in the representation of non-living nouns, for which shape and function are often related than in the representation of living things, for which distinguishing features tend to be idiosyncratic.

According to both approaches, a small amount of damage would mostly affect concepts with idiosyncratic features and few inter-correlated features, but more excessive damage would affect entire feature clusters and therefore impair entire groups of concepts that share these clusters. Consequently, both approaches predict a relation between the amount of damage to the semantic system and relative performance with concepts from different semantic domains. However, the two approaches differ in which semantic domain they predict would be more affected by small and large amounts of damage to the semantic system. The Gonnerman et al. approach predicts that with small amounts of damage to the semantic system, non-living nouns would be more impaired than living nouns and that later in the disease this pattern would switch. Moss, Tyler, and Jenkins make exactly the opposite prediction.

Because the role of feature inter-correlation is a matter of debate, and because most of the empirical work in this area has not considered verb performance, it is important to test empirically whether the relation between features can explain performance patterns in both nouns and verbs. Thus, the third and final specific goal of this work was to test predictions of specific feature-based accounts. Accounts based on the sensory-functional distinction predict an association between patients’ relative performance with nouns vs. verbs and (a) their relative performance with non-living vs. living nouns, and (b) their relative performance with instrument vs. manner verbs. Accounts that are based on feature inter-correlation predict an association between patients’ naming accuracy and (a) their relative impairment with non-living vs. living nouns, and (b) their relative impairment with instrument vs. manner verbs.

To summarize, the present research addressed three main questions:

  • 1.

    Is verb performance in AD compatible with graceful degradation in a general feature-based framework such that relative levels of naming performance are preserved across different categories?

  • 2.

    Is verb performance in AD compatible with graceful degradation in a general feature-based framework in terms of error pattern progression (i.e., super-ordinate errors  contrast coordinate errors  cross-category errors  “do not know” errors)?

  • 3.

    Do patterns of noun and verb category impairments support the sensory-functional models of Bird et al., 2000, Parris and Weekes, 2001, and/or the feature inter-correlation models of Gonnerman et al., 1997, Tyler and Moss, 2001?

We addressed these questions using a timed picture naming task because this task has been used to successfully assess lexical semantic performance in AD patients (e.g., Gonnerman et al., 1997). The relative simplicity of this task allowed us to employ a much larger set of stimuli than would have been possible with more complex stimuli such as animations. Because response times are not likely to show ceiling effects in the same way as accuracy scores, we also measured naming latencies (Druks et al., 2006). The pictures were selected from six non-living noun categories, six living noun categories, six instrument verb categories, and six manner verb categories. Throughout the rest of this paper we shall use the term “semantic domain” to distinguish between living and non-living objects and between instrument and manner verbs. We shall use the term “semantic category” to refer to individual categories such as “zoo animals” or “vehicle motion” verbs. We shall also use the term “word class” to distinguish between nouns and verbs. To ensure sufficient performance variability and avoid ceiling effects, pictures varied in naming difficulty and included pictures which pilot data indicated were difficult to name.

Section snippets

Participants

Fourteen patients with AD and fourteen healthy elderly normal controls (EN) participated in this study. Table 1 shows participants’ demographic and Mini-Mental State Exam (MMSE) scores. The two groups were matched for age, t(13) = 1.6, n.s., and years of education, t(13) = −1.68, n.s., but the patients had lower MMSE scores, t(13) = 1.6, p < .001. Participants were paid for their participation. The AD patients were diagnosed with probable Alzheimer’s disease using the NINCDS-ADRDA criteria (McKhann et

Results and discussion

In order to ensure that our results were not affected by a baseline noun vs. verb impairment in the AD patients, we examined naming accuracy for nouns and verbs in the two groups (Fig. 1a). Accuracy data were analyzed once with participants as a random factor (F1) and once with items as a random factor (F2). The participants analysis used a mixed design ANOVA with Group (EN, AD) as a between factor and Word Class (Noun, Verb) as a within factor. The items analysis used a mixed design ANOVA with

General discussion

By using a large set of items that varied in difficulty, we were able to examine noun and verb performance in both healthy control participants and patients with AD in a manner that minimized ceiling effects in the healthy control group and floor effects in the AD group. As expected, AD patients’ naming difficulties resulted in lower accuracy and longer naming latencies than the healthy control participants across all conditions. Although the AD patients in our study demonstrated worse

Conclusion

We found strong evidence that the semantic system is governed by an underlying featural system that operates similarly but not identically, for noun and verb representation. Widespread damage to this system, as is the case in Alzheimer’s disease, is detectable across the entire semantic system, along with selective and related deficits to specific categories for both nouns and verbs. For nouns, the faster degradation of living compared to non-living nouns is compatible with explanations that

Acknowledgments

This research was supported by NIH grant RO1 AG-11774. Alison Flipse and Mariko Taki provided invaluable help in stimuli preparation, testing, and data coding. We thank the participants and their families for their generous contribution of time and effort. Portions of this work were presented at the annual meetings of the Academy of Aphasia (Vienna, Austria, October 2003) and the Cognitive Science Society (Chicago, August 2004). Some aspects of the noun naming data were also reported in Aronoff

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