BRAIN
AND
r.ANGUAGE
43, 169-189 (1992)
Speech Production, Syntax Comprehension, and Cognitive Deficits in Parkinson’s Disease PHILIP LIEBERMAN, EDWARD KAKO,* JOSEPH FRIEDMAN,+ GARY TAJCHMAN, LIANE S. FELDMAN, AND ELSA B. JIMINEZ Department of Cognitive and Linguistic Sciences, Brown University; *Yale University; and TDepartment of Clinical Neurosciences, Brown University, and Department of Neurology, Roger Williams General Hospital
Speech samples were obtained that were analyzed for voice onset time (VOT) for 40 nondemented English speaking subjects, 20 with mild and 20 with moderate Parkinson’s disease. Syntax comprehension and cognitive tests were administered to these subjects in the same test sessions. VOT disruptions for stop consonants in syllable initial position, similar to those noted for Broca’s aphasia, occurred for nine subjects. Longer response times and errors in the comprehension of syntax as measured by the Rhode Island Test of Sentence Comprehension (RITLS) also occurred for these subjects. Anovas indicate that the VOT overlap subjects had significantly higher syntax error rates and longer response times on the RITLS than the VOT nonoverlap subjects-F(1, 70) = 12.38, p < 0.0008; F(1, 70) = 7.70, p < 0.007, respectively. The correlation between the number of VOT timing errors and the number of syntax errors was significant. (r = 0.6473, p < 0.01). VOT overlap subjects also had significantly higher error rates in cognitive tasks involving abstraction and the ability to maintain a mental set. Prefrontal cortex, acting through subcortical basal ganglia pathways, is a component of the neural substrate that regulates human speech production, syntactic ability, and certain aspects of cognition. The deterioration of these subcortical pathways may explain similar phenomena in Broca’s aphasia. Results are discussed in relation to “modular” theories. 0 1992 Academic Press. Inc.
INTRODUCTION
Human linguistic ability has traditionally been associated with specific regions of the cortex on the basis of clinicopathologic studies of aphasia. Indeed, many linguists continue to claim that human syntactic ability (which they equate with human language) derives from a neocortical “module” which is “encapsulated,” i.e., functionally and morphologically Address reprint requests to Philip Lieberman at the Department of Cognitive and Linguistic Sciences, Box 1978, Brown University, Providence, RI 02912. 169 0093-934X/92 $5.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.
170
~IEBERMAN
ET AL.
distinct from other modules that govern other aspects of human behavior (Fodor, 1983, Chomsky, 1986). No homologue to the hypothetic~ syntax module supposedly exists in any other species. According to one theory (Bickerton, 1990), the cortical syntax module evolved by means of a single genetic change that dramatically modified the human neocortex, creating cortical maps encoding grammatical relations and a “syntactic” wiring diagram. However, this neurophysiological model is not consistent with many early studies of aphasia-producing lesions which pointed to subcortical involvement in language (Marie, 1926). A number of recent studies show that permanent, “big,” Broca’s aphasia is the consequence of extensive subcortical damage (Stuss & Benson, 1986). Indeed, subcortical damage that disrupts the connections from Broca’s area, leaving it intact, can result in Broca-like speech production deficits (Naeser, Alexander, HelmsEstabrooks, Levine, Laughlin, & Geschwind, 1982; Benson & Geschwind, 1972, pp. 206-207; Stuss & Benson, 1986, p. 161; Alexander, Naeser, & Palumbo, 1987; Metter, Kempler, Jackson, Hanson, Mazziotta, & Phelps, 1989). Metter, Riege, Hanson, Phelps, and Kuhl (1984) found that metabolic activity in the caudate nucleus, which forms part of a pathway to the prefrontal cortex (Parent, 1986), correlated with mean writing and reading scores of the Boston Diagnostic Aphasia Examination (BDAE) and with the speaking and comprehension factor scores of the Porch Index of Communicative Ability (PICA). Moreover, Metter and his associates (1987) note hypometabolism in prefrontal cortex with Broca’s aphasia and conclude that the behavioral deficits of Broca’s aphasia~eneral “difficulty in motor sequencing and executing motor speech tasks,” as well as “language comprehension abnormalities”-derive from damage to neural pathways to prefrontal cortex. However, lesions are generally not so localized nor is the resolution of present imaging techniques adequate to determine whether damage limited to subcortical basal ganglia pathways to prefrontal cortex can cause speech, language, and cognitive disturbances. Since Parkinson’s disease (PD), a neurodegenerative disease is primarily limited to subcortical basal ganglia structures, it can serve as an “experiment-in-nature” to resolve the question of whether the linguistic deficits associated with Broca’s aphasia can derive from damage to subcortical pathways to prefrontal cortex.’ ’ Although cortical pathology also occurs in patients with PD these cortical changes do not appear to be a consequence of PD since similar changes occur in age-matched controls (Jellinger, 1990). Cortical changes are uncommon in PD unless Alzheimer’s occurs as well (Jellinger, 199O),or when Lewy bodies occur in widespread fashion throughout the cortex. In this case the diagnosis is distinct being “diffuse Lewy body disease,” a rare disorder, rather than PD (Jellinger, 1990; Xuereb, Tomlinson, Irving, Perry, Blessed, & Perm, 1990).
PARKINSON’S DISEASE
171
It is important to note that the hypothesis that we are testing is not that prefrontal cortex is the brain’s “language organ.” The hypothesis that we shall test, and the data that we shall discuss, point to a model in which specialized neural structures operate in different behavioral domains through different neural pathways (Mesulam, 1985). In the case of speech production and syntax, we will be testing the claim that basal ganglia “circuits” between Broca’s area and prefrontal cortex regulate the precise motor sequencing necessary for speech, and the application of syntactic “rules” (Lieberman, 1991). The data that we will discuss also address another issue, whether the brain bases of linguistic ability are modules distinct from cognition. Since prefrontal cortex is implicated in cognitive functions involving the abstraction of concepts (Stuss & Benson, 1986), we might expect to find cognitive as well as linguistic deficits occurring in our subjects. This would not be surprising since previous studies have demonstrated cognitive deficits in Parkinson’s disease (Cummings & Benson, 1984; Flowers & Robertson, 1985) similar to ones associated with frontal lobe damage (Benson & Geschwind, 1972). It is also important to note that we do not expect to find that all PD patients will have linguistic deficits. Although Parkinson’s disease can potentially affect many of the cortical pathways that involve the basal ganglia (Parent, 1986), the specific circuits involving Broca’s region and prefrontal cortex may not be affected, particularly in the early stages of the disease process. We, therefore, will make use of one of the attested speech motor deficits of Broca’s aphasia as a “probe” that may indicate whether PD has affected pathways involving Broca’s area in a particular subject. PREVIOUS STUDIES
Speech, language, and cognitive deficits previously have been noted in PD, although the results of different studies conflict. Several studies have described patients’ difficulty in performing tasks of lexical and sentence disambiguation, confrontation naming, generative naming, and syntactic judgments (Bayles & Boone, 1982; Bayles & Tomoeda, 1983; Bayles, 1984; Tweedy, Langer, & McDowell, 1982). In contrast, other studies show no consistent difference in vocabulary; PD patients in some situations use fewer words than normal control subjects, but use more words in other circumstances (Pirozzolo, Hansch, Mortimer, Webster, & Kuskowski, 1982). Deficits reflecting syntax appear to be more consistent; differences in the syntactic complexity of the spontaneous speech of PD patients as well as increases in the number and duration of the short These patients are often demented. population.
We excluded demented patients from our PD subject
172
LIEBERMAN
ET AL.
“hesitation” pauses that occur in the flow of speech were noted by Illes, Metter, Hanson, and Iritani (1988) and Illes (1989). Deficits in the comprehension of syntax coupled with some cognitive loss were noted for moderate PD (Hoehn & Yahr (1967), stage III) subjects by Lieberman et al. (1990). Deficits in the comprehension of syntactically complex sentences were noted by Grossman et al. (1991) for 73% of a sample of 22 PD patients (Hoehn & Yahr stages I and II). Grossman and his associates also found that 63% of these patients had praxis deficits in performing tasks from the BDAE. Independent neurophysiologic data indicate that these deficits, as is the case for Broca’s aphasia, may result from damage to subcortical basal ganglia pathways to frontal cortex (Albert, Feldman, & Willis, 1974); positron emission tomography (PET) studies which show prefrontal hyopometabolism in PD demonstrate that BG pathways to prefrontal cortex have been degraded (Metter et al., 1984, 1987). The speech production measure that we will use as a “probe’‘-that is, a measure that identifies PD subjects exhibiting the “difficulty in motor sequencing” noted for Broca’s aphasia-is voice onset time (VOT). VOT is the time that elapses between the onset of phonation and the burst that occurs on the release of a stop consonant (Lisker & Abramson, 1964). “Voiced” sounds such as [b] , [d] , and [g] are produced with a short VOT, “unvoiced” [p], [t], and [k] with long VOTs. Acoustic analysis reveals that Broca’s aphasics merge VOT for voiced and unvoiced stop consonants (Blumstein, Cooper, Goodglass, Statlender, & Gottlieb, 1980). Moreover, recent data on Broca’s aphasia show that these VOT overlap deficits occurred in subjects who sustained damage to both Broca’s region and subcortical pathways; CT scan data for these subjects show damage to subcortical areas including putamen, caudate nucleus, and the internal capsule (Baum, Blumstein, Naeser, & Palumbo, 1990). PROCEDURES Subjects. Forty out-patients with idiopathic Parkinson’s disease without evidence of aphasia were tested at Roger Williams Hospital in Providence, Rhode Island. Twenty were evaluated as having stage III PD according to the Hoehn-Yahr scale (Hoehn & Yahr, 1967); these patients were labeled “moderate.” The other 20 were evaluated as having stage I-II PD and were labeled “mild.” Subjects in the moderate population ranged in age from 56 to 81 years, with a mean age of 69.1 years. Subjects in the mild population ranged in age from 45 to 72 years, with a mean age of 61.0 years. All subjects were free from dementia.’ Neither the neurologist (JF), who spent significant amounts of time with them, or their families had noted evidence of cognitive decline. All subjects except 6 moderates and 2 milds were native monolingual speakers of English. The patients for whom this information was available (some were enrolled in a NINCDS protocol that limited access to this information) were either unmedicated or on stable programs of treatment-none showed “onoff” patterns of fluctuating short-term PD symptoms. Tables 1A and 1B show the case profiles for all subjects including the duration of their PD (from time of initial diagnosis), level of education, and the type of medication being taken at the time of testing.
173
PARKINSON’S DISEASE TABLE 1A CASE PROFILES OF SUBJECTS IN THE MODERATE
Subject Age Sex 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
72 79 74 68 64 67 58 81 75 74 73 57 62 67 60 77 56 78 69 71
M M F M M F M M M M M M M M M M F M M M
Level of education 12th grade B.A. 10th grade 12th grade 9th grade Some college 9th grade B.A. 12th grade B.A. B.A. M.A. 12th grade 9th grade Ph.D. 8th grade Some college 11th grade B.A. 8th grade
POPULATION
Duration of Age First acquired disease language English (years) Armenian English French English English French French English English English English English English English English Yiddish English English English Polish
4-5 6-7 4 7
12
23
10 16 5 14
AND
r.ANGUAGE
43, 169-189 (1992)
Speech Production, Syntax Comprehension, and Cognitive Deficits in Parkinson’s Disease PHILIP LIEBERMAN, EDWARD KAKO,* JOSEPH FRIEDMAN,+ GARY TAJCHMAN, LIANE S. FELDMAN, AND ELSA B. JIMINEZ Department of Cognitive and Linguistic Sciences, Brown University; *Yale University; and TDepartment of Clinical Neurosciences, Brown University, and Department of Neurology, Roger Williams General Hospital
Speech samples were obtained that were analyzed for voice onset time (VOT) for 40 nondemented English speaking subjects, 20 with mild and 20 with moderate Parkinson’s disease. Syntax comprehension and cognitive tests were administered to these subjects in the same test sessions. VOT disruptions for stop consonants in syllable initial position, similar to those noted for Broca’s aphasia, occurred for nine subjects. Longer response times and errors in the comprehension of syntax as measured by the Rhode Island Test of Sentence Comprehension (RITLS) also occurred for these subjects. Anovas indicate that the VOT overlap subjects had significantly higher syntax error rates and longer response times on the RITLS than the VOT nonoverlap subjects-F(1, 70) = 12.38, p < 0.0008; F(1, 70) = 7.70, p < 0.007, respectively. The correlation between the number of VOT timing errors and the number of syntax errors was significant. (r = 0.6473, p < 0.01). VOT overlap subjects also had significantly higher error rates in cognitive tasks involving abstraction and the ability to maintain a mental set. Prefrontal cortex, acting through subcortical basal ganglia pathways, is a component of the neural substrate that regulates human speech production, syntactic ability, and certain aspects of cognition. The deterioration of these subcortical pathways may explain similar phenomena in Broca’s aphasia. Results are discussed in relation to “modular” theories. 0 1992 Academic Press. Inc.
INTRODUCTION
Human linguistic ability has traditionally been associated with specific regions of the cortex on the basis of clinicopathologic studies of aphasia. Indeed, many linguists continue to claim that human syntactic ability (which they equate with human language) derives from a neocortical “module” which is “encapsulated,” i.e., functionally and morphologically Address reprint requests to Philip Lieberman at the Department of Cognitive and Linguistic Sciences, Box 1978, Brown University, Providence, RI 02912. 169 0093-934X/92 $5.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.
170
~IEBERMAN
ET AL.
distinct from other modules that govern other aspects of human behavior (Fodor, 1983, Chomsky, 1986). No homologue to the hypothetic~ syntax module supposedly exists in any other species. According to one theory (Bickerton, 1990), the cortical syntax module evolved by means of a single genetic change that dramatically modified the human neocortex, creating cortical maps encoding grammatical relations and a “syntactic” wiring diagram. However, this neurophysiological model is not consistent with many early studies of aphasia-producing lesions which pointed to subcortical involvement in language (Marie, 1926). A number of recent studies show that permanent, “big,” Broca’s aphasia is the consequence of extensive subcortical damage (Stuss & Benson, 1986). Indeed, subcortical damage that disrupts the connections from Broca’s area, leaving it intact, can result in Broca-like speech production deficits (Naeser, Alexander, HelmsEstabrooks, Levine, Laughlin, & Geschwind, 1982; Benson & Geschwind, 1972, pp. 206-207; Stuss & Benson, 1986, p. 161; Alexander, Naeser, & Palumbo, 1987; Metter, Kempler, Jackson, Hanson, Mazziotta, & Phelps, 1989). Metter, Riege, Hanson, Phelps, and Kuhl (1984) found that metabolic activity in the caudate nucleus, which forms part of a pathway to the prefrontal cortex (Parent, 1986), correlated with mean writing and reading scores of the Boston Diagnostic Aphasia Examination (BDAE) and with the speaking and comprehension factor scores of the Porch Index of Communicative Ability (PICA). Moreover, Metter and his associates (1987) note hypometabolism in prefrontal cortex with Broca’s aphasia and conclude that the behavioral deficits of Broca’s aphasia~eneral “difficulty in motor sequencing and executing motor speech tasks,” as well as “language comprehension abnormalities”-derive from damage to neural pathways to prefrontal cortex. However, lesions are generally not so localized nor is the resolution of present imaging techniques adequate to determine whether damage limited to subcortical basal ganglia pathways to prefrontal cortex can cause speech, language, and cognitive disturbances. Since Parkinson’s disease (PD), a neurodegenerative disease is primarily limited to subcortical basal ganglia structures, it can serve as an “experiment-in-nature” to resolve the question of whether the linguistic deficits associated with Broca’s aphasia can derive from damage to subcortical pathways to prefrontal cortex.’ ’ Although cortical pathology also occurs in patients with PD these cortical changes do not appear to be a consequence of PD since similar changes occur in age-matched controls (Jellinger, 1990). Cortical changes are uncommon in PD unless Alzheimer’s occurs as well (Jellinger, 199O),or when Lewy bodies occur in widespread fashion throughout the cortex. In this case the diagnosis is distinct being “diffuse Lewy body disease,” a rare disorder, rather than PD (Jellinger, 1990; Xuereb, Tomlinson, Irving, Perry, Blessed, & Perm, 1990).
PARKINSON’S DISEASE
171
It is important to note that the hypothesis that we are testing is not that prefrontal cortex is the brain’s “language organ.” The hypothesis that we shall test, and the data that we shall discuss, point to a model in which specialized neural structures operate in different behavioral domains through different neural pathways (Mesulam, 1985). In the case of speech production and syntax, we will be testing the claim that basal ganglia “circuits” between Broca’s area and prefrontal cortex regulate the precise motor sequencing necessary for speech, and the application of syntactic “rules” (Lieberman, 1991). The data that we will discuss also address another issue, whether the brain bases of linguistic ability are modules distinct from cognition. Since prefrontal cortex is implicated in cognitive functions involving the abstraction of concepts (Stuss & Benson, 1986), we might expect to find cognitive as well as linguistic deficits occurring in our subjects. This would not be surprising since previous studies have demonstrated cognitive deficits in Parkinson’s disease (Cummings & Benson, 1984; Flowers & Robertson, 1985) similar to ones associated with frontal lobe damage (Benson & Geschwind, 1972). It is also important to note that we do not expect to find that all PD patients will have linguistic deficits. Although Parkinson’s disease can potentially affect many of the cortical pathways that involve the basal ganglia (Parent, 1986), the specific circuits involving Broca’s region and prefrontal cortex may not be affected, particularly in the early stages of the disease process. We, therefore, will make use of one of the attested speech motor deficits of Broca’s aphasia as a “probe” that may indicate whether PD has affected pathways involving Broca’s area in a particular subject. PREVIOUS STUDIES
Speech, language, and cognitive deficits previously have been noted in PD, although the results of different studies conflict. Several studies have described patients’ difficulty in performing tasks of lexical and sentence disambiguation, confrontation naming, generative naming, and syntactic judgments (Bayles & Boone, 1982; Bayles & Tomoeda, 1983; Bayles, 1984; Tweedy, Langer, & McDowell, 1982). In contrast, other studies show no consistent difference in vocabulary; PD patients in some situations use fewer words than normal control subjects, but use more words in other circumstances (Pirozzolo, Hansch, Mortimer, Webster, & Kuskowski, 1982). Deficits reflecting syntax appear to be more consistent; differences in the syntactic complexity of the spontaneous speech of PD patients as well as increases in the number and duration of the short These patients are often demented. population.
We excluded demented patients from our PD subject
172
LIEBERMAN
ET AL.
“hesitation” pauses that occur in the flow of speech were noted by Illes, Metter, Hanson, and Iritani (1988) and Illes (1989). Deficits in the comprehension of syntax coupled with some cognitive loss were noted for moderate PD (Hoehn & Yahr (1967), stage III) subjects by Lieberman et al. (1990). Deficits in the comprehension of syntactically complex sentences were noted by Grossman et al. (1991) for 73% of a sample of 22 PD patients (Hoehn & Yahr stages I and II). Grossman and his associates also found that 63% of these patients had praxis deficits in performing tasks from the BDAE. Independent neurophysiologic data indicate that these deficits, as is the case for Broca’s aphasia, may result from damage to subcortical basal ganglia pathways to frontal cortex (Albert, Feldman, & Willis, 1974); positron emission tomography (PET) studies which show prefrontal hyopometabolism in PD demonstrate that BG pathways to prefrontal cortex have been degraded (Metter et al., 1984, 1987). The speech production measure that we will use as a “probe’‘-that is, a measure that identifies PD subjects exhibiting the “difficulty in motor sequencing” noted for Broca’s aphasia-is voice onset time (VOT). VOT is the time that elapses between the onset of phonation and the burst that occurs on the release of a stop consonant (Lisker & Abramson, 1964). “Voiced” sounds such as [b] , [d] , and [g] are produced with a short VOT, “unvoiced” [p], [t], and [k] with long VOTs. Acoustic analysis reveals that Broca’s aphasics merge VOT for voiced and unvoiced stop consonants (Blumstein, Cooper, Goodglass, Statlender, & Gottlieb, 1980). Moreover, recent data on Broca’s aphasia show that these VOT overlap deficits occurred in subjects who sustained damage to both Broca’s region and subcortical pathways; CT scan data for these subjects show damage to subcortical areas including putamen, caudate nucleus, and the internal capsule (Baum, Blumstein, Naeser, & Palumbo, 1990). PROCEDURES Subjects. Forty out-patients with idiopathic Parkinson’s disease without evidence of aphasia were tested at Roger Williams Hospital in Providence, Rhode Island. Twenty were evaluated as having stage III PD according to the Hoehn-Yahr scale (Hoehn & Yahr, 1967); these patients were labeled “moderate.” The other 20 were evaluated as having stage I-II PD and were labeled “mild.” Subjects in the moderate population ranged in age from 56 to 81 years, with a mean age of 69.1 years. Subjects in the mild population ranged in age from 45 to 72 years, with a mean age of 61.0 years. All subjects were free from dementia.’ Neither the neurologist (JF), who spent significant amounts of time with them, or their families had noted evidence of cognitive decline. All subjects except 6 moderates and 2 milds were native monolingual speakers of English. The patients for whom this information was available (some were enrolled in a NINCDS protocol that limited access to this information) were either unmedicated or on stable programs of treatment-none showed “onoff” patterns of fluctuating short-term PD symptoms. Tables 1A and 1B show the case profiles for all subjects including the duration of their PD (from time of initial diagnosis), level of education, and the type of medication being taken at the time of testing.
173
PARKINSON’S DISEASE TABLE 1A CASE PROFILES OF SUBJECTS IN THE MODERATE
Subject Age Sex 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
72 79 74 68 64 67 58 81 75 74 73 57 62 67 60 77 56 78 69 71
M M F M M F M M M M M M M M M M F M M M
Level of education 12th grade B.A. 10th grade 12th grade 9th grade Some college 9th grade B.A. 12th grade B.A. B.A. M.A. 12th grade 9th grade Ph.D. 8th grade Some college 11th grade B.A. 8th grade
POPULATION
Duration of Age First acquired disease language English (years) Armenian English French English English French French English English English English English English English English Yiddish English English English Polish
4-5 6-7 4 7
12
23
10 16 5 14
