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Observation
January 1998

Functional Brain Imaging in Apraxia

Author Affiliations

From the Departments of Neurology (Drs Kareken and Farlow), Psychiatry (Drs Kareken and Unverzagt), and Radiology (Drs Caldemeyer and Hutchins), Indiana University School of Medicine, and the Richard L. Roudebush Veterans Affairs Medical Center (Dr Kareken), Indianapolis.

Arch Neurol. 1998;55(1):107-113. doi:10.1001/archneur.55.1.107
Abstract

Background  An extensive literature describes structural lesions in apraxia, but few studies have used functional neuroimaging. We used positron emission tomography (PET) to characterize relative cerebral glucose metabolism in a 65-year-old, right-handed woman with progressive decline in ability to manipulate objects, write, and articulate speech.

Objective  To characterize functional brain organization in apraxia.

Design and Methods  The patient underwent a neurological examination, neuropsychological testing, magnetic resonance imaging, and fludeoxyglucose F 18 PET. The patient's magnetic resonance image was coregistered to her PET image, which was compared with the PET images of 7 right-handed, healthy controls. Hemispheric regions of interest were normalized by calcrine cortex.

Results  Except for apraxia and mild grip weakness, results of the neurological examination were normal. There was ideomotor apraxia of both hands (command, imitation, and object) and buccofacial apraxia. The patient could recognize meaningful gestures performed by the examiner and discriminate between his accurate and awkward pantomime. The magnetic resonance image showed moderate generalized atrophy and mild ischemic changes. Positron emission tomographic scans showed abnormal fludeoxyglucose F 18 uptake in the posterior frontal, supplementary motor, and parietal regions, the left affected more than the right. Focal metabolic deficit was present in the angular gyrus, an area hypothesized to store conceptual knowledge of skilled movement.

Conclusions  Greater parietal than frontal physiological dysfunction and preserved gesture recognition are not consistent with the theory that knowledge of limb praxis is stored in the dominant parietal cortex. Gesture comprehension may be more diffusely distributed.

APRAXIA IS a

disorder of skilled movement not caused by weakness, akinesia, deafferentation, abnormal tone or posture, movement disorders, intellectual deterioration, poor comprehension, or uncooperativeness.1

Patients with ideomotor apraxia are unable to pantomime on command symbolic gestures (eg, saluting) or use of tools, and their movements are characterized by errors in posture, spatial orientation, and joint coordination.24 Analogous movement defects in the face, lips, tongue, cheeks, larynx, and pharynx (eg, blowing out a match or whistling) are termed buccofacial apraxia.1 Although a number of studies have described the structural lesions that result in apraxia, little work has described the functional network of brain regions that become compromised.

Lesion research suggests that left intrahemispheric lesions are most commonly responsible for apraxia in both hands. Because right hemisphere lesions are not known to induce apraxia,5,6 the left hemisphere appears dominant for the storage and execution of learned movements. Although both anterior and posterior lesions in the left hemisphere produce apraxia, patients with parietal lesions often have difficulty comprehending gesture, and discriminating between accurately and poorly performed pantomime gestures.7,8 Occipital lesions that disconnect visual association areas from the parietal lobe may lead to impaired gesture imitation, but otherwise normal praxis.9 Although still unable to execute gesture, patients with frontal lesions are better able to accurately discriminate good from bad pantomime, and comprehend gesture in others.7,8 Some authors7,10 therefore propose that the left supramarginal and angular gyri contain visuokinesthetic motor programs that are implemented by premotor areas in the left hemisphere. The superior parietal lobule (Brodmann areas 5 and 7) might also play a role by translating motor programs into somatosensory cues that guide limb movement.11 Buccofacial apraxia is less well studied than limb apraxia. Lesions related to this disorder have been found in the frontal operculum, anterior insula, and striatum.12,13

In contrast to the extensive study of lesion location in apraxia, there has been little use of physiological imaging to describe functional brain organization. Physiological imaging is important because structural lesions have remote functional effects that computed tomography and magnetic resonance imaging (MRI) cannot detect.14 Although some investigations1518 have found apraxia to relate to parietal defects in glucose metabolism or blood flow, only 1 of these reports18 related regional functional activity to gesture production and comprehension. Rapcsak et al18 recently studied a woman with slowly progressive bilateral limb apraxia using single photon emission computed tomography. Despite having ideomotor apraxia, her conceptual knowledge of tool use and limb movement was intact. Single photon emission computed tomography, nonetheless, demonstrated severe biparietal hypoperfusion, a finding that appears inconsistent with the hypothesis that conceptual knowledge of limb praxis and gesture comprehension are mediated primarily by the inferior parietal lobule.7,10

We used positron emission tomography (PET) to map the cortical distribution of relative glucose metabolism in a 65-year-old woman with a 4-year progressive decline in manipulating objects, writing, and speech articulation. In the absence of any clear structural abnormality, we sought to determine the relative contribution of frontal and parietal cortical glucose metabolism to her gesture production and comprehension.

SUBJECTS, DESIGN, AND METHODS
PATIENT AND SUBJECTS

The patient was a 65-year-old, high school–educated, right-handed woman who presented to the Indiana Alzheimer Disease Center in Indianapolis. Approximately 4 years earlier, she experienced the insidious onset of difficulty speaking and writing. These symptoms gradually progressed, and she became unable to properly manipulate silverware and small items (eg, buttons or jewelry). She gradually became unable to perform her household chores, including management of family finances. At the time of her clinic visit, she had difficulty finding and articulating words, but continued to read and understand television programs.

Seven healthy control subjects from the Indiana Alzheimer Disease Center–PET database were selected for imaging comparison (mean age, 69 years; age range, 56-79 years). The controls had no evidence of cerebral or neuropsychological abnormality. Informed consent was obtained from all subjects after the nature of the procedure had been fully explained.

MATERIALS AND PROCEDURE
Clinical Examinations

The patient underwent neurological and neuropsychological examinations (Table 1 and Table 2). Apraxia examination involved testing gesture production and comprehension. To test production, the patient was asked to pantomime on command 10 intransitive gestures (waving goodbye, hitchhike, salute, beckon "come here," signal stop, finger to lips for "shsh," finger tapping, "ok" sign, 2 "ok" signs linked together, and the "peace" or "V" for victory sign), 8 transitive gestures (opening a door with a key, flipping a coin, opening a ketchup bottle, stirring coffee with a spoon, and using a screwdriver, hammer, scissors, and handsaw), and 8 buccofacial movements (cough, sniff, puff out cheeks, wink, stick out tongue, blow a kiss, blow out a match, and suck on a straw). To test gesture comprehension, the patient was asked to discriminate 4 target gestures from foils (using a hammer, waving goodbye, shooting a basketball, and flipping a coin) and 4 precise target gestures from the same gestures performed clumsily and with a body part as object (brushing teeth and using a hammer, scissors, and key).

Table 1. 
Neuropsychological Test Results*
Neuropsychological Test Results*
Table 2. 
Aphasia Examination*
Aphasia Examination*
Imaging

The PET studies were performed on a whole body PET tomograph (Siemens 951/31R, 6-mm full-width half-maximum intrinsic resolution) in a dimly lit room with subjects supine, resting, and eyes open. Regional cerebral glucose uptake was measured with 2-fludeoxyglucose F 18 (10-mCi intravenous bolus), and images were reconstructed to 9-mm spatial resolution. The PET images for all subjects were spatially registered in the horizontal plane along the anterior commissure–posterior commissure line. A whole brain proton density–weighted MRI scan of the patient's head was acquired in the axial plane, and coregistered with her PET image volume using an iterative procedure that minimizes the least-squared difference between the MRI and PET image volumes. Magnetic resonance images were unavailable for the controls. The regions of interest analyses were performed on the PET images by one of us (D.A.K.), normalizing hemispheric regions of interest by the average of left and right calcrine cortex.

Five regions of interest were delineated: anterior frontal (FA) (corresponding to the dorsolateral prefrontal cortex), posterior frontal (FP) (corresponding to premotor and primary motor regions), parietal, caudate-putamen (CP), and supplementary motor area (SMA). All regions were divided into left (L) and right (R). The central sulcus was approximated by a line just posterior to the thalamus as viewed on the midsagittal image (Figure 1, A, plane a). Although this landmark confounds slightly the actual division between frontal and parietal cortex, it was a reliable landmark. The division between FA and FP was defined on the axial image with a line through the center of the 2 caudate heads. This was an easily identifiable, reliable landmark, and constitutes the approximate division between premotor cortex (Brodmann area 6) and the cortex anterior to it28 (Figure 1, A, plane c). Insular cortex was excluded from FP and cingulate cortex from FA. For the parietal regions of interest, the cuneus and lateral occipital gyri were excluded in slices inferior to the parieto-occiptial sulcus (Figure 1, A, plane d). Tracing of frontal and parietal regions of interest began on an axial plane just dorsal to the thalamus (Figure 1, C, plane e). On the coronal images this plane passed through both sylvian fissures (Figure 1, B, plane e). Tracings were made of the cortical ribbon with a computer mouse on the axial images at each of 5 planes dorsal to the thalamus, with an interplane interval of 5 pixels (≈10 mm) (Figure 1, C).

Figure 1.
A through C, Region of interest definition in 1 healthy control. Axial image A shows the planes approximating the central sulcus (a), interhemispheric fissure (b), the division between anterior and posterior frontal region (c), and the plane that excludes the occipital regions from the parietal region (d) in sections below the parieto-occipital fissure. Coronal image B is taken at plane a. Sagittal image C depicts the approximate location of the 5 axial sections, beginning with the base plane e, that were averaged to create the frontal and parietal regions of interest. The shaded area in the sagittal image represents the approximate region of the supplementary motor area.

A through C, Region of interest definition in 1 healthy control. Axial image A shows the planes approximating the central sulcus (a), interhemispheric fissure (b), the division between anterior and posterior frontal region (c), and the plane that excludes the occipital regions from the parietal region (d) in sections below the parieto-occipital fissure. Coronal image B is taken at plane a. Sagittal image C depicts the approximate location of the 5 axial sections, beginning with the base plane e, that were averaged to create the frontal and parietal regions of interest. The shaded area in the sagittal image represents the approximate region of the supplementary motor area.

The SMA was approximated with a right triangle on the sagittal image (Figure 1, C, shaded area). The vertical line of the right angle (posterior boundary) was placed at the anterior-posterior division line, and the horizontal line (ventral boundary) was placed at the midpoint between the corpus callosum and the vertex of the cerebrum. The hypotenuse followed the cortex along the edge of the interhemispheric sulcus. As defined, SMA probably includes most of Brodmann area 6 and at least some of Brodmann area 8 (see reference 28). Two planes of SMA (one on the mesial surface of the interhemispheric sulcus, one 4-mm lateral) were traced in each hemisphere and averaged. Tracings of CP were performed at a single plane of the axial image that traversed the midpoint of the caudate heads as visualized in the coronal images.

RESULTS
CLINICAL EXAMINATIONS

Neurological examination revealed an awake, alert, verbally dysfluent woman who was well oriented except for the name of the hospital and the date. Finger to nose, rapid alternating movements, and heel to shin were all intact. There were occasional random movements of her hands. A hand dynamometer showed her grip strength to be mildly weak bilaterally, but tone and strength were otherwise normal in the upper and lower extremities. Reflexes were 2-3+ and symmetric, and there were no Babinski signs. Results of a sensory examination of light touch, pain, and proprioception were unremarkable. Magnetic resonance imaging revealed moderate cortical atrophy that was mildly asymmetric, the left hemisphere being more atrophic than the right. Mild small vessel ischemic disease was also present in the periventricular white matter, but there were no focal lesions present.

Results of neuropsychological and aphasia examinations appear in Table 1 and Table 2. Verbal IQ was low average and Performance IQ was borderline. Abstraction and mental flexibility in novel problem solving were normal on the Wisconsin Card Sorting Test. Category Test errors were average for age and education (T score, 4520). Visuomotor tracking (Trail Making) was mildly slow (T scores, 32 and 35 for parts A and B, respectively29). Memory and visual perception were intact. Tactile perception (finger gnosis and graphesthesis) was impaired bilaterally. Right-left orientation was normal. The patient performed simple addition and subtraction with variable accuracy, and her score on the mathematics section of the Wide Range Achievement Test, third edition, was in the eighth percentile.

The Boston Diagnostic Aphasia Examination revealed no deficit in auditory or written language comprehension, but showed marked motor language impairment. Speech was halting, labored, and marked by frequent literal and semantic paraphasias. Asked about her work, she offered the following response:

Well, I was, ah re... tired before that, but ah, I worked, ah be ... ah ... at a ... ah ... let me think, at ... ah ... I ... place where people, ah ... a ... cars ... ah ... in Michigan. I did I didn't ... I was in the ... ah office, and ah working in a ... on a ... c ... on a cc ... cc ... con ... con ... contuter. And before that it was on a ... I ... before... I got that mon ... I was working in a ... s ... savings an a loa... loan.

Letter (C, F, and L) and category (animals) fluency were defective. Although visual confrontation naming was normal, the patient had difficulty retrieving the name of an object when given its description. Spelling was also impaired, even when using plastic block letters and spelling aloud (both of which circumvented her motor apraxia). The patient was able to produce slowly handwritten block letters, with occasional letter malformation.

APRAXIA TESTING

On command, the patient performed successfully only 2 of 10 intransitive gestures. She improved only minimally when asked to imitate the examiner. Pantomime of transitive movement (use of tools) was likewise impaired in both hands (1 of 8 correct). There was no improvement with imitation, and only mild improvement with actual objects. During intransitive gestures, the patient's most frequent problem was her inability to internally configure the fingers on her hand. She was acutely aware of her errors, and many times used 1 hand to try (unsuccessfully) to force her fingers into the correct configuration. In both intransitive and transitive gestures, she additionally experienced trouble orienting her hand and arms correctly toward the imagined tool or object (eg, pointing at her mouth when making the shsh gesture). In 6 of the 8 transitive gestures, her movements were themselves incorrect. These configural and movement errors persisted with imitation. Content errors were also evident. When pantomiming the shsh gesture, the patient blew on her finger as if blowing out a match. When pantomiming scissors, she moved her mouth synergistically to the rhythm of opening and closing the scissors (which she could not make her hand do). There was only 1 perseverative error in which she carried the movements of one action into the movements of another. Her ability to recognize movements in the examiner, and to discriminate between his accurate and poor performance, was unaffected (4 of 4 and 4 of 4, respectively). The patient also had difficulty pantomiming and imitating buccofacial gestures, although her performance was better than her limb movements (4 of 6 correct, most of which were awkward and slow). She was, however, unable to perform any of the oral agility items on the Boston Diagnostic Aphasia Examination to the minimum number of trial repetitions (purse lips, open and close mouth, retract lips, tongue to alternate corners of mouth, protrude tongue, and tongue to upper and lower teeth).

FUNCTIONAL IMAGING

Positron emission tomography showed the patient to have fludeoxyglucose F 18 uptake in the distribution of the controls for R-FA, L-FA, R-FP, R-P, and CP bilaterally. The fludeoxyglucose F 18 uptake fell outside the distribution of the controls in L-FP, L-P, and SMA bilaterally. The left-right discrepancy in frontal and parietal regions appeared greater in the patient (Figure 2). Thus, the patient's left hemisphere showed greater loss than the right, and reduced fludeoxyglucose F 18 uptake was distributed in a posterior frontal and parietal distribution. Visual examination of the patient's coregistered PET and MRI scans showed focal reductions of fludeoxyglucose F 18 uptake in the region of the left angular and supramarginal gyri (Figure 3). Focal reductions were also present in the left insular cortex and the inferior precentral gyrus (Figure 3, A).

Figure 2.
Fludeoxyglucose F 18 uptake in regions of interest, normalized by the average of left and right calcrine cortex (patient vs healthy elderly controls, n=7). R indicates right; L, left; FA, frontal-anterior; FP, frontal-posterior; P, parietal; CP, caudate-putamen; and SMA, supplementary motor area.

Fludeoxyglucose F 18 uptake in regions of interest, normalized by the average of left and right calcrine cortex (patient vs healthy elderly controls, n=7). R indicates right; L, left; FA, frontal-anterior; FP, frontal-posterior; P, parietal; CP, caudate-putamen; and SMA, supplementary motor area.

Figure 3.
Three sections (A through C) of the patient's positron emission tomographic and coregistered proton density magnetic resonance images showing regions of relative hypometabolism. The inferior and middle frontal gyri fall in the anterior-frontal regions defined on the positron emission tomographic scan. In image B, note hypometabolism falling in the region of the angular and supramarginal gyri.

Three sections (A through C) of the patient's positron emission tomographic and coregistered proton density magnetic resonance images showing regions of relative hypometabolism. The inferior and middle frontal gyri fall in the anterior-frontal regions defined on the positron emission tomographic scan. In image B, note hypometabolism falling in the region of the angular and supramarginal gyri.

COMMENT

This 65-year-old woman with progressive speech and motor difficulty had significant limb ideomotor and buccofacial apraxia, but spared gesture comprehension. A comprehensive neuropsychological examination showed that this occurred in the context of normal memory, mental flexibility, abstraction, language comprehension, and visuospatial perception. With absent focal structural lesions and global cognitive impairments to complicate interpretation of regional metabolic dysfunction, PET revealed asymmetric reduced fludeoxyglucose F 18 uptake, with greater loss in the left FP and parietal regions. Focal metabolic loss specifically involved the angular and supramarginal gyri, which corresponded with the patient's impaired tactile perception, agraphia, and dyscalculia. These findings appear inconsistent with the theory that the inferior parietal lobule, in particular the supramarginal and angular gyri, contain the visuokinesthetic motor programs for skilled movement.7,10

There are several explanations for why gesture comprehension might be preserved with parietal lobe dysfunction. First, gesture recognition and discrimination may simply be an easier task, and visuokinesthetic engrams stored in the left inferior parietal lobule may not have degraded sufficiently to impair gesture comprehension.18 Alternatively, a more detailed examination of gesture comprehension might have revealed comprehension defects. However, the imaging results are similar to those of another case, described by Rapcsak et al.18 These authors also described a patient with a slowly progressive ideomotor apraxia, severe biparietal atrophy, and widespread parietal hypoperfusion demonstrated with single photon emission computed tomography. Despite this patient's extensive reduction in parietal lobe perfusion, a comprehensive examination revealed well-preserved gesture comprehension and conceptual knowledge of limb movements.

Gesture comprehension may therefore be more diffusely distributed. Evidence for this comes from Bonda et al,30 who studied the regional cerebral blood flow of healthy individuals observing meaningful human gestures. In addition to increased regional cerebral blood flow in the intraparietal sulcus, they found that regional cerebral blood flow increases in the ventral temporo-occipital cortex and prestriate cortex in the right hemisphere, and the caudal superior temporal sulcus, ventral temporo-occipital cortex, and prestriate cortex of the left. This corresponds to nonhuman primate studies of reciprocal connections between the inferior parietal lobule and temporal lobe visual areas (eg, TPO-2, TPO-3, TPO-4, MT, superior temporal sulcus),3134 where cells respond selectively to forms of movement.3539

Another account for the observed findings and parietal lobe mediation of gesture comprehension could be that this patient's apraxia results from frontal lobe dysfunction, but reduced parietal fludeoxyglucose F 18 uptake is secondary to loss of afferent projections to the parietal lobe from premotor and supplementary motor areas. 40,41 This does not provide a complete account of the data in the present case, as the patient's finger agnosia, dysgraphesthesis, dyscalculia, and spelling impairment strongly implicate dysfunction of the left inferior parietal lobule.4244 Finally, stroke represents the most frequently studied cause of apraxia. In both our patient and the one described by Rapcsak et al,18 apraxia was the result of insidious disease. It is possible that functional brain reorganization is different in disorders of sudden onset.

Other findings in this study are nonetheless consistent with current anatomic models of praxis. Early studies of regional cerebral blood flow and cortical recordings show that SMA plays a key role in motor planning.4547 In this patient, regions corresponding to the premotor area and SMA were more severely affected than the dorsolateral prefrontal cortex. Buccofacial apraxia is frequently the result of frontal lesions, and in this case it may be secondary to reduced functional integrity in the insular and inferior precentral cortex.12,13 In fact, Dronkers48 recently found that patients with speech apraxia have lesions in the precentral gyrus of the insula, which may coordinate oral motor planning and articulation.

The diagnosis of our patient is uncertain, but the onset of symptoms and course resembles that of corticobasal degeneration (CBD), a slowly progressive disorder whose initial symptoms include apraxia.4955 There are, nonetheless, differences between our patient and others with confirmed CBD. Unlike our patient, all 30 cases of CBD studied by Rinne et al53 presented with limb rigidity 5 years after onset, and a substantial number exhibited dystonia (83%), myoclonus (57%), and alien limb (50%). Some patients with neuropathological confirmation of CBD, however, have delayed onset of the typical motor features.56 Our patient also exhibited apparently normal fludeoxyglucose F 18 uptake in the caudate and putamen. Other studies of CBD have reported asymmetric glucose metabolism57 and blood flow in the basal ganglia,58 as well as decreased basal ganglia uptake of dopaminergic tracers.59,60 Fluorodopa F 18 might therefore have been a more sensitive measure of basal ganglia function in our patient. Our result of asymmetric posterior frontal and parietal functional fludoexyglucose F 18 uptake was, however, consistent with CBD.5759,61,62 Many patients with CBD also present with a pattern of neuropsychological deficit that resembles a dysexecutive syndrome.55 Apart from apraxia, dysgraphia, dyscalculia, and deficits in sensory perception, our patient had no significant cognitive deficit. It is also true that patients with clinical diagnoses of CBD are neuropathologically diverse, and that those with concomitant dementia also satisfy neuropathological criteria for Parkinson disease, Alzheimer disease, progressive supranuclear palsy, and hippocampal sclerosis.63 Patients without these concomitant criteria may initially present without significant cognitive loss. With specific regard to CBD and anatomic and cognitive models of apraxia, Blin et al57 reported that all their CBD patients with apraxia were able to recognize the examiner's gestures. The most severe metabolically defective regions in these patients were in sensorimotor, temporal, and parietal association areas.

The findings of this study underline the importance of functional imaging in the investigation of the cortical architecture of skilled movement. Structural lesion research suggests that the angular and supramarginal gyri mediate gesture comprehension. Although the conclusions that can be drawn from a case study are limited, functional imaging in this and other work suggests that gesture comprehension may be spared with significant functional disruption of the posterior parietal lobule. Future research in apraxia should be targeted at developing more systematic functional imaging studies that analyze extended networks of cortical and subcortical regions that mediate action production and comprehension. Patients with early symptoms of CBD may constitute an advantageous population of study, since apraxic symptoms may sometimes occur in the absence of other confounding cognitive disturbances.63

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Article Information

Accepted for publication July 28, 1997.

This study was supported by the Physiologic Imaging Research Center of the Indiana University School of Medicine, the Indiana Alzheimer Disease Center (P30 AG10133), and the Richard L. Roudebush Veterans Affairs Medical Center, Indianapolis.

We gratefully acknowledge the assistance of Vincent Mathews, MD, the staff of the Indiana University PET facility, Marilyn M. Wagner, PhD, of Frazier Rehabilitation Center (Louisville, Ky) for portions of the neuropsychological test data, and Julie C. Stout, PhD, for valuable comments on a previous version of the manuscript.

Reprints: David A. Kareken, PhD, Neuropsychology Section (RI 5999C), Department of Neurology, Indiana University School of Medicine, Indianapolis, IN 46202 (e-mail: dkareken@.iupui.edu).

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