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A unitary semantics account of reverse concreteness effects in semantic dementia
Brain and Language 103 (2007) 8–249 www.elsevier.com/locate/b&l
A unitary semantics account of reverse concreteness effects in semantic dementia Jamie Reilly *, Jonathan E. Peelle, Murray Grossman Department of Neurology, 3 Gates Building, University of Pennsylvania School of Medicine, Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA 19104-4283, USA
One of the most consistent paradigms in which processing advantages appear for concrete words is lexical decision: adults are typically faster to discriminate concrete over abstract words when matched on other psycholinguistic variables such word frequency, length, and phonological neighborhood density (van Schie, Wijers, Mars, Benjamins, & Stowe, 2005). Dual coding theory holds that separate visual and verbal semantic systems are dedicated to the representation of abstract and concrete words (Paivio, 1991). Concrete words reference an additional semantic network that aids in their retrieval. However, dual coding theory cannot adequately account for reversals of the concreteness effect (i.e., faster decision times and better naming for abstract words) seen in semantic dementia (SD) since damage to the visual semantic system should logically produce equivalent impairment for abstract and concrete words if both word types are represented within a dissociable verbal semantic system. SD patients experience profound anomia associated with semantic impairment that transcends modality of presentation, suggesting degradation of a unitary semantic system (Bozeat, Lambon Ralph, Patterson, Garrard, & Hodges, 2000). In line with this finding, we hypothesize that a single amodal store subserves abstract and concrete word meaning and that these amodal representations index the breadth of knowledge that informs semantic memory, including verbally- and perceptually-mediated associates. Atrophy in SD progressively compromises anterior temporal structures that index semantic features and ventral temporal lobe structures that compose the pathway of visual object recognition. We hypothesize that as SD progresses, perceptually salient visual features will be less accessible, and the concreteness effect will reverse. We tested this hypothesis via an auditory lexical decision task among SD patients who vary in disease severity. Methods Participants were 7 males (mean age = 67.14; SD = 9.65) diagnosed with SD in accord with published criteria (McKhann et al., 2001), listed in Table 1. Patient performance was contrasted with a control group composed of 10 healthy age-matched adults (mean age = 63.10; SD = 9.70).
*
Corresponding author. E-mail address: [email protected] (J. Reilly).
doi:10.1016/j.bandl.2007.07.057
Stimuli included 40 nouns with concreteness values obtained from the MRC Psycholinguistic database (Coltheart, 1981) and 40 pronounceable pseudowords. Concrete and abstract nouns (20 of each) were matched for word frequency and had average concreteness ratings of 574 and 355 respectively on a 100–700 scale. Words were recorded by a native English speaker and presented binaurally over headphones. Participants viewed a monitor with an unchanging display that asked ‘‘Is this a word?’’. Participants were instructed to signal their choice via button press as quickly and as accurately as possible. In reaction time (RT) analyses, incorrect responses were eliminated, as were latencies >2 SD, beyond the pooled set of observations. Results Lexical decision accuracy was comparable across conditions. Among latencies (see Table 1), there was a significant 2-way interaction between group and word concreteness [F(1, 79) = 4.85, p < .05]. SD patients showed a reverse concreteness effect in lexical decision with longer latencies by a margin of 234 ms to discriminate concrete nouns [t(38) = 2.11, p < .05], whereas controls showed an advantage in recognition for concrete nouns of 22.95 ms. This RT difference among controls was significant by items but not by participant. For each patient, an RT difference score was calculated by subtracting latencies for concrete from abstract nouns, and these scores were correlated with measures of naming integrity and dementia severity. As predicted, patients showed a graded reverse concreteness effect as a function of dementia severity. There was a strong negative correlation between RT difference score and naming integrity as measured by performance on the BNT [r(6) = .67, p = .05] (Kaplan, Goodglass, & Weintraub, 1983). There was also a strong correlation between RT difference score and dementia severity as measured by MMSE [r(6) = .68, p = .04, one-tailed] (Folstein, Folstein, & McHugh, 1975). Discussion We tested the hypothesis that progressive damage to ventral and anterior temporal lobe structures associated with SD would result in a graded advantage for concrete over abstract nouns. This was indeed the case: as SD patients’ disease severity increased, the advantage of concrete over abstract words decreased. These results are consistent with a model of
Abstract / Brain and Language 103 (2007) 8–249
87
Table 1 Lexical decision results and patient demographics Patient
Age
BNT
MMSE
Response time (ms) Low imageability
High imageability
Difference (low high)
AI LL-1 LG JF SB JR LL-2
74 71 50 63 69 80 63
14 13 10 10 4 3 2
27 24 29 21 22 6 21
1020.56 1333.45 1010.58 2033.13 1027.32 3114.67 2699.33
1030.10 1156.63 1012.65 2481.07 969.63 3965.00 3508.23
9.54 176.82 2.07 447.93 57.68 850.33 560.80
Note. BNT, Boston Naming Test using 15 items. MMSE, Mini Mental State Examination.
semantic memory in which amodal semantic knowledge is stored in a unified manner, and in which perceptually salient information, such as visual features, can be activated upon semantic retrieval to aid processing. Abstract words may be more resilient to the loss of feature knowledge because their meaning is less reliant upon perceptual features and more upon linguistically mediated associations. This unitary theory of abstract–concrete word representation may also account for reliance upon concreteness observed in deep dysphasia. References Bozeat, S., Lambon Ralph, M. A., Patterson, K., Garrard, P., & Hodges, J. R. (2000). Non-verbal semantic impairment in semantic dementia. Neuropsychologia, 38, 1207–1215. Coltheart, M. (1981). The MRC psycholinguistic database. Quarterly Journal of Experimental Psychology, 33(a), 497–505.
Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini-Mental state: A practical method for grading the state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198. Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston naming test. Philadelphia: Lea and Febiger. McKhann, G., Trojanowski, J. Q., Grossman, M., Miller, B. L., Dickson, D., & Albert, M. (2001). Clinical and pathological diagnosis of frontotemporal dementia: Report of a work group on frontotemporal dementia and Pick’s disease. Archives of Neurology, 58, 1803–1809. Paivio, A. (1991). Dual coding theory: Retrospect and current status. Canadian Journal of Psychology, 45(3), 255–287. van Schie, H. T., Wijers, A. A., Mars, R. B., Benjamins, J. S., & Stowe, L. A. (2005). Processing of visual semantic information to concrete words: Temporal dynamics and neural mechanisms indicated by event-related brain potentials. Cognitive Neuropsychology, 22(3–4), 364–386.
A unitary semantics account of reverse concreteness effects in semantic dementia Jamie Reilly *, Jonathan E. Peelle, Murray Grossman Department of Neurology, 3 Gates Building, University of Pennsylvania School of Medicine, Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA 19104-4283, USA
One of the most consistent paradigms in which processing advantages appear for concrete words is lexical decision: adults are typically faster to discriminate concrete over abstract words when matched on other psycholinguistic variables such word frequency, length, and phonological neighborhood density (van Schie, Wijers, Mars, Benjamins, & Stowe, 2005). Dual coding theory holds that separate visual and verbal semantic systems are dedicated to the representation of abstract and concrete words (Paivio, 1991). Concrete words reference an additional semantic network that aids in their retrieval. However, dual coding theory cannot adequately account for reversals of the concreteness effect (i.e., faster decision times and better naming for abstract words) seen in semantic dementia (SD) since damage to the visual semantic system should logically produce equivalent impairment for abstract and concrete words if both word types are represented within a dissociable verbal semantic system. SD patients experience profound anomia associated with semantic impairment that transcends modality of presentation, suggesting degradation of a unitary semantic system (Bozeat, Lambon Ralph, Patterson, Garrard, & Hodges, 2000). In line with this finding, we hypothesize that a single amodal store subserves abstract and concrete word meaning and that these amodal representations index the breadth of knowledge that informs semantic memory, including verbally- and perceptually-mediated associates. Atrophy in SD progressively compromises anterior temporal structures that index semantic features and ventral temporal lobe structures that compose the pathway of visual object recognition. We hypothesize that as SD progresses, perceptually salient visual features will be less accessible, and the concreteness effect will reverse. We tested this hypothesis via an auditory lexical decision task among SD patients who vary in disease severity. Methods Participants were 7 males (mean age = 67.14; SD = 9.65) diagnosed with SD in accord with published criteria (McKhann et al., 2001), listed in Table 1. Patient performance was contrasted with a control group composed of 10 healthy age-matched adults (mean age = 63.10; SD = 9.70).
*
Corresponding author. E-mail address: [email protected] (J. Reilly).
doi:10.1016/j.bandl.2007.07.057
Stimuli included 40 nouns with concreteness values obtained from the MRC Psycholinguistic database (Coltheart, 1981) and 40 pronounceable pseudowords. Concrete and abstract nouns (20 of each) were matched for word frequency and had average concreteness ratings of 574 and 355 respectively on a 100–700 scale. Words were recorded by a native English speaker and presented binaurally over headphones. Participants viewed a monitor with an unchanging display that asked ‘‘Is this a word?’’. Participants were instructed to signal their choice via button press as quickly and as accurately as possible. In reaction time (RT) analyses, incorrect responses were eliminated, as were latencies >2 SD, beyond the pooled set of observations. Results Lexical decision accuracy was comparable across conditions. Among latencies (see Table 1), there was a significant 2-way interaction between group and word concreteness [F(1, 79) = 4.85, p < .05]. SD patients showed a reverse concreteness effect in lexical decision with longer latencies by a margin of 234 ms to discriminate concrete nouns [t(38) = 2.11, p < .05], whereas controls showed an advantage in recognition for concrete nouns of 22.95 ms. This RT difference among controls was significant by items but not by participant. For each patient, an RT difference score was calculated by subtracting latencies for concrete from abstract nouns, and these scores were correlated with measures of naming integrity and dementia severity. As predicted, patients showed a graded reverse concreteness effect as a function of dementia severity. There was a strong negative correlation between RT difference score and naming integrity as measured by performance on the BNT [r(6) = .67, p = .05] (Kaplan, Goodglass, & Weintraub, 1983). There was also a strong correlation between RT difference score and dementia severity as measured by MMSE [r(6) = .68, p = .04, one-tailed] (Folstein, Folstein, & McHugh, 1975). Discussion We tested the hypothesis that progressive damage to ventral and anterior temporal lobe structures associated with SD would result in a graded advantage for concrete over abstract nouns. This was indeed the case: as SD patients’ disease severity increased, the advantage of concrete over abstract words decreased. These results are consistent with a model of
Abstract / Brain and Language 103 (2007) 8–249
87
Table 1 Lexical decision results and patient demographics Patient
Age
BNT
MMSE
Response time (ms) Low imageability
High imageability
Difference (low high)
AI LL-1 LG JF SB JR LL-2
74 71 50 63 69 80 63
14 13 10 10 4 3 2
27 24 29 21 22 6 21
1020.56 1333.45 1010.58 2033.13 1027.32 3114.67 2699.33
1030.10 1156.63 1012.65 2481.07 969.63 3965.00 3508.23
9.54 176.82 2.07 447.93 57.68 850.33 560.80
Note. BNT, Boston Naming Test using 15 items. MMSE, Mini Mental State Examination.
semantic memory in which amodal semantic knowledge is stored in a unified manner, and in which perceptually salient information, such as visual features, can be activated upon semantic retrieval to aid processing. Abstract words may be more resilient to the loss of feature knowledge because their meaning is less reliant upon perceptual features and more upon linguistically mediated associations. This unitary theory of abstract–concrete word representation may also account for reliance upon concreteness observed in deep dysphasia. References Bozeat, S., Lambon Ralph, M. A., Patterson, K., Garrard, P., & Hodges, J. R. (2000). Non-verbal semantic impairment in semantic dementia. Neuropsychologia, 38, 1207–1215. Coltheart, M. (1981). The MRC psycholinguistic database. Quarterly Journal of Experimental Psychology, 33(a), 497–505.
Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini-Mental state: A practical method for grading the state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198. Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston naming test. Philadelphia: Lea and Febiger. McKhann, G., Trojanowski, J. Q., Grossman, M., Miller, B. L., Dickson, D., & Albert, M. (2001). Clinical and pathological diagnosis of frontotemporal dementia: Report of a work group on frontotemporal dementia and Pick’s disease. Archives of Neurology, 58, 1803–1809. Paivio, A. (1991). Dual coding theory: Retrospect and current status. Canadian Journal of Psychology, 45(3), 255–287. van Schie, H. T., Wijers, A. A., Mars, R. B., Benjamins, J. S., & Stowe, L. A. (2005). Processing of visual semantic information to concrete words: Temporal dynamics and neural mechanisms indicated by event-related brain potentials. Cognitive Neuropsychology, 22(3–4), 364–386.