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Neurocase
2003, Vol. 9, No. 5, pp. 421–435
1355-4794/03/0905–421$16.00
# Swets & Zeitlinger
A Double Dissociation Between the Meanings
of Action Verbs and Locative Prepositions
David Kemmerer1,2 and Daniel Tranel2
1
Department of Audiology and Speech Sciences and Department of Psychological Sciences, Purdue University,
West Lafayette, IN, USA, and 2Division of Cognitive Neuroscience, University of Iowa College of Medicine,
Iowa City, IA, USA
Abstract
We describe two patients who manifested opposite patterns of performance on test batteries that evaluated
production, comprehension, and semantic analysis of action verbs on the one hand (e.g. smile, wave, run) and locative
prepositions on the other (e.g. in, on, over). JP failed all of the verb tests but passed all of the preposition tests,
suggesting impaired knowledge of the meanings of action verbs but intact knowledge of the meanings of locative
prepositions. In contrast, RR exhibited the reverse dissociation: he passed many of the verb tests but failed all of the
preposition tests, suggesting mostly intact knowledge of the meanings of action verbs but impaired knowledge of the
meanings of locative prepositions. This behavioral double dissociation reflects the fact that the two categories of words
differ along several conceptual parameters. To a large extent, the patients exhibited a neuroanatomical
double dissociation as well, since JP’s lesion is predominantly in the left frontal operculum whereas RR’s is
predominantly in the left inferior parietal lobe and the posterior superior temporal region. This constitutes preliminary
evidence that the meanings of action verbs and locative prepositions are represented by partially independent
neural networks in the brain.
Introduction
Numerous studies have investigated the neural architecture of
word meaning, and evidence from several approaches – the
lesion method, functional imaging, and electrophysiology –
has been converging on the view that lexicosemantic structures belonging to different conceptual domains are treated
differently in the brain. Most of these studies have focused on
nouns that refer to concrete entities such as animals, fruits/
vegetables, tools, persons, and body parts (see reviews by
Martin and Chao, 2001; Forde and Humphreys, 2002). Comparatively less research has been devoted to verbs for physical
actions (see reviews by Druks, 2002; Cappa and Perani,
2003), and even less attention has been paid to other word
classes, such as prepositions that designate spatial locations
(e.g. Kemmerer and Tranel, 2000a; Damasio et al., 2001).
Here we present new experimental data suggesting that the
meanings of action verbs and locative prepositions have
partially independent neural bases. Specifically, we report
two brain-damaged patients, one of whom has impaired
knowledge of the semantic structures encoded by action verbs
but intact knowledge of the semantic structures encoded by
locative prepositions, and the other of whom has the opposite
dissociation. Before describing the experiments, we review
pertinent background material on the meanings and neural
substrates of the two word classes.
The meanings of action verbs
and locative prepositions
Although some verbs refer to abstract states and events (e.g.
exist, remain, increase, elapse), the prototypical function of
verbs in all languages is to denote physical actions, that is,
situations in which an agent, such as a person or animal,
engages in certain kinds of dynamic bodily movement. Most
contemporary theories of verb semantics assume that causal
structure constitutes the major skeletal framework around
which verb meanings are built (e.g. Van Valin and LaPolla,
1997; Croft, 1998; Rappaport and Levin, 1998). The simplest
verbs represent situations in which an agent performs a purely
body-internal activity that does not necessarily bring about
any changes in other entities (e.g. sing, laugh, wave, jog).
Other verbs are more complex insofar as they express activities that do affect other entities in certain ways, such as by
inducing a change of state (e.g. slice, engrave, wash, kill) or a
change of location (e.g. pour, twist, load, smear).
Correspondence to: David Kemmerer, Department of Audiology and Speech Sciences, 1353 Heavilon Hall, Purdue University, West Lafayette,
IN 47907-1353, USA. Tel: þ1-765-494-3826; Fax: þ1-765-494-0771; e-mail: kemmerer@purdue.edu
422
D. Kemmerer and D. Tranel
In addition to the basic organizing factor of causal structure, the meanings of action verbs can be analyzed and
compared in terms of the various semantic fields that they
characterize. Levin (1993) sorted over 3,000 English verbs
(the majority of which were action verbs) into approximately
50 classes and 200 subclasses. Representative classes include
verbs of throwing (e.g. fling, hurl, lob, toss), verbs of contact
by impact (e.g. pound, swat, tap, poke), verbs of creation (e.g.
build, assemble, sculpt, weave), and verbs of ingesting (e.g.
eat, chew, gobble, devour). The verbs in a given class collectively provide a richly detailed, multidimensional categorization of the relevant semantic field by making distinctions,
sometimes of a remarkably fine-grained nature, along a
number of different parameters. For instance, verbs of
destruction are distinguished by the composition of the entity
to be destroyed (e.g. tear vs. smash), the degree of force (e.g.
tear vs. rip), and the extent of deformation (e.g. tear vs.
shred). Similarly, for verbs of locomotion distinctions are
made regarding manner of motion (e.g. skip, limp, tiptoe,
march), rate of motion (e.g. walk, jog, run, sprint), and the
attitude of the agent (e.g. sneak, strut, sashay, trudge).
The verbs in a given class are also organized according to
principled semantic relations such as the following (Fellbaum,
1998): synonymy, in which two verbs have nearly identical
meanings (e.g. shout and yell); antonymy, in which two verbs
have opposite meanings (e.g. lengthen and shorten); hyponymy,
in which oneverb is at a higher taxonomic level than another (e.g.
talk and lecture); and cohyponymy, in which two verbs are at
roughly the same taxonomic level (e.g. bow and curtsey).
A final point about the meanings of action verbs is that they
vary considerably across languages. First, languages differ in
the idiosyncractic semantic features of verbs (e.g. Newman,
1997, 2002). For instance, Wagiman (an Australian Aboriginal
language) has an unusual verb (more precisely, a coverb), murr,
which means ‘‘to walk along in the water looking for something
with one’s feet’’ (Wilson, 1999). In addition, languages differ in
the size of their verb lexicons. Some languages, like Yimas and
Kalam (both in New Guinea), have very small inventories of
only about 100 verb roots, so that verb serialization is required
to express complex events. Thus, the conceptual event
expressed in English by ‘‘I fetched some firewood’’ requires
no less than six Kalam verb roots (Pawley, 1993):
yad am mon p-wk d ap ay-p-yn
1SG go wood hit-break hold come put-PERF-1SG
‘‘I fetched some firewood’’
Another type of variation involves the encoding of motion
events (e.g. Talmy, 1985; Wienold, 1995; Slobin, in press). In
manner-incorporating languages (e.g. English, German,
Russian, Swedish, Chinese), manner of motion is typically
encoded by the verb (e.g. walk, saunter, creep, crawl), while
path information is optionally expressed by prepositional
phrases (e.g. across the street). By contrast, in path-incorporating languages (e.g. Modern Greek, Spanish, Japanese,
Turkish, Hindi), the verb usually encodes direction of motion
(e.g. Modern Greek: beno ‘‘move in’’, vgeno ‘‘move out’’,
aneveno ‘‘move up’’, kateveno ‘‘move down’’), while manner
information is optionally expressed by prepositional phrases
or gerunds (e.g. me ta podia/perpatontas ‘‘on foot/walking’’).
This brief review of crosslinguistic diversity raises the possibility that the meanings of action verbs are language-specific
semantic structures, perhaps distinct from the kinds of nonlinguistic action concepts that are employed in behavioral
planning, perceptual recognition, and inferential reasoning
(Gennari et al., 2002, Papafragou et al., 2002).
Action verbs and locative prepositions are similar insofar as
they share the conceptual domain of space: physical actions
necessarily unfold in space, and locations are also necessarily
defined in terms of space. However, the two types of words
differ semantically in several important ways. In contrast to
action verbs, locative prepositions do not encode dynamic
processes; instead, they designate static spatial relationships
between objects. In the standard case, two objects are
involved – the ‘‘figure’’, which is an object whose location
is the focus of attention, and the ‘‘landmark’’, which is an
object that serves as a point of reference for locating the
figure. For example, in the sentence There’s a fly in your soup,
the noun-phrase a fly specifies the figure, the noun-phrase your
soup specifies the landmark, and the preposition in specifies
the nature of the spatial relationship between them.
Whereas action verbs number in the thousands and fall into
a wide variety of classes and subclasses (at least in English),
there are only a small number of locative prepositions
(roughly 50 in English) and they comprise just two main
classes – geometrical and projective (e.g. Herskovits, 1986;
Garrod et al., 1999). Geometrical prepositions encode spatial
relationships in terms of a combination of topological and
functional features – for instance, in expresses ‘‘containment’’, on expresses both ‘‘contiguity’’ and ‘‘support,’’
around expresses ‘‘encirclement’’, and through expresses
‘‘penetration’’. Projective prepositions refer to spatial locations that are extended from the major dimensional axes of the
landmark – thus, above and below designate relations of
superiority and inferiority with respect to the vertical axis
of the landmark, and in front of and in back of (or behind)
designate relations of anteriority and posteriority with respect
to the front/back axis of the landmark.
Given that there are significantly fewer locative prepositions than action verbs, it is not surprising that the former
words exhibit a much broader range of application than the
latter (although, to be sure, verbs can also be quite polysemous). For example, on typically refers to a situation in
which the figure is in direct contact with the landmark and is
supported by it horizontally through gravity, such as a cup on a
table, a child on a swing, a car on a road, etc. However, it is
still possible to use on when one of the typical conditions is
violated, as in the following situations: a cup on a table even
though books and papers intervene (no direct contact between
figure and landmark); a picture on a wall (vertical support by
virtue of attachment instead of horizontal support by virtue of
gravity); and a stripe on a shirt (the figure is not really
supported by the landmark since it is part of the landmark).
Double dissociation between verbs and prepositions
Accounting for the remarkable flexibility of locative prepositions has proven to be a challenge for semantic analysis
(Sandra and Rice, 1995).
Yet another interesting difference between action verbs and
locative prepositions involves the amount of detail that can be
encoded in the semantic structures of the words. Whereas
action verbs are capable of expressing very subtle nuances of
meaning, locative prepositions are confined to expressing
spatial relationships in terms of very schematic structural
properties of the objects involved (e.g. Herskovits, 1986;
Landau and Jackendoff, 1993; Lindstromberg, 1998). Usually
the most important properties are general geometric features
(e.g. volumes, surfaces, lines, points), axial structure (e.g. top/
bottom, front/back, left/right), and quantity (e.g. between
requires two landmark objects, and among requires an aggregate). For the most part, metrical details are ignored, such as
the particular sizes, shapes, and orientations of objects, or the
precise distances between them (see Brown, 1994, for an
important exception to this generalization).
Finally, as with action verbs, the meanings of locative
prepositions vary a great deal across languages. An instructive
example is to look at how English, Finnish, Dutch, and Spanish
describe the following situations: a cup on a table, an apple in a
bowl, and a handle on a door (Bowerman, 1996; Bowerman and
Choi, 2001). In English the same preposition, on, is used to
refer to the ‘‘cup on table’’ and ‘‘handle on door’’ situations
because both of them share the features of contact and support,
and a different preposition, in, is used for the ‘‘apple in bowl’’
situation because it involves containment. Finnish is sensitive
to a slightly different distinction. One case-marker, -ssa, specifies what might be called intimate contact, a semantic category that includes both containment and attachment, so it is
used for both the ‘‘apple in bowl’’ and ‘‘handle on door’’
situations. A different case-marker, -lla, specifies non-intimate
contact, which includes horizontal support through gravity, so
it is used for the ‘‘cup on table’’ situation. As for Dutch and
Spanish, they go in opposite semantic directions. Dutch opts
for maximal segregation, employing three different prepositions – op, in, and aan – for the three situations, and Spanish opts
for maximal generalization, using just one preposition – en – for
the three situations. This crosslinguistic diversity suggests that
when people talk about the spatial world, they must conceptualize their experience in ways that reflect the unique perspective captured by the inventory of expressions in the given
language. Furthermore, this in turn suggests that the meanings
of prepositions may be distinct from the kinds of spatial
representations that are used for non-linguistic purposes such
as perceptual categorization and motor control (Kemmerer,
1999; Kemmerer and Tranel, 2000a; Crawford et al., 2000;
Munnich et al., 2001).
The neural substrates of action verbs
and locative prepositions
Very little is currently known about the specific neural
structures that underlie the meanings of action verbs and
423
locative prepositions. However, several recent studies (summarized below) suggest that, at the level of large-scale neural
systems, the meanings of both types of words are subserved by
various components of the so-called dorsal stream, predominantly in the left hemisphere. This is what one would expect,
given that the dorsal stream has been alternately characterized
as the ‘‘how’’ system and the ‘‘where’’ system, the term
‘‘how’’ deriving from evidence that the system plays an
essential role in the visuomotor control of action (Goodale
and Milner, 1992), and the term ‘‘where’’ deriving from
evidence that the system also contributes to representing
the locations of objects in space (Ungerleider and Mishkin,
1982).
Damasio et al. (2001) report a PET study in which subjects
named static pictures of actions with the appropriate verbs and
also named static pictures of spatial relationships with the
appropriate prepositions. Action naming recruited the left
frontal operculum, the left inferior parietal region (supramarginal and angular gyri), and bilaterally the posterior-most
aspect of the middle temporal gyrus and the bordering occipital cortex (i.e. the area known as MT – e.g. Dumoulin et al.,
2000). The left frontal activation could reflect many aspects
of verb processing, including the retrieval of phonological
forms (Tranel et al., 2001; Hillis et al., 2002b), the retrieval of
grammatical category information (Shapiro et al., 2001), and
the retrieval of conceptual knowledge (McCarthy and
Warrington, 1985; Daniele et al., 1994; Bak et al., 2001;
Tranel et al., in press). Especially intriguing evidence for
more widespread involvement of the left frontal lobe in
representing the meanings of body-part-specific action verbs
comes from recent studies suggesting that face-, arm-, and
leg-related verbs (e.g. yawn, grab, and jump) are linked with
the corresponding inferior, lateral, and superior sectors of
somatotopically mapped premotor cortices (Buccino et al.,
2001; Pulvermuller et al., 2001). Regarding the activation that
Damasio et al. (2001) observed in the left inferior parietal
region, it was significantly greater for naming actions performed with tools (e.g. write) than for naming actions performed without tools (e.g. walk), and other studies have also
related this brain region to conceptual knowledge for tool
manipulation and for various kinds of object-directed hand
actions within peripersonal space (e.g. Binkofski et al., 1999;
Chao and Martin, 2000; Buccino et al., 2001). As for the
posterior middle temporal region (area MT), it is activated
when subjects view static pictures of objects that imply
motion, such as an athlete running versus an athlete standing
still (Kourtzi and Kanwisher, 2000; Senior et al., 2000), and
numerous studies have found this area (and the area just
anterior and dorsal to it) to be associated with the meanings
of action verbs (Wise et al., 1991; Martin et al., 1995; Fiez
et al., 1996; Warburton et al., 1996; Kable et al., 2002; Tranel
et al., in press).
For the task of naming spatial relationships with prepositions, Damasio et al. (2001) found the largest and strongest
activation to be in the left supramarginal gyrus; smaller and
weaker activations were observed in the left frontal opercular
424
D. Kemmerer and D. Tranel
and polar regions. It is not clear how each of these neural
structures contributes functionally to the complex naming
process; however, the results are consistent with lesion studies
which have found that damage in the left frontoparietal
territory is associated with impaired processing of locative
prepositions, including specifically the meanings of these
words (see also Friederici, 1982, 1985; Friederici et al.,
1982; Grodzinsky, 1988; Tesak and Hummer, 1994;
Kemmerer and Tranel, 2000a; Froud, 2001; Kemmerer, submitted; Tranel and Kemmerer, submitted). Furthermore, an
fMRI study found activation in the parietal lobes bilaterally
when subjects read sentences containing locative prepositions
(Carpenter et al., 1999). It is also noteworthy that the left
inferior parietal region has been linked with the representation
of schematic categorical spatial relationships of the sort that
are typically encoded by locative prepositions (e.g. Laeng,
1994; Kosslyn et al., 1998; Baciu et al., 1999).
The current study
As the preceding review indicates, action verbs and locative
prepositions have similarities as well as differences at both
semantic and neural levels of description. The two kinds of
words are semantically similar because they both involve the
conceptual domain of space, and this commonality is apparently reflected in closely related neural circuits in the left
frontal opercular region and the left supramarginal gyrus. And
yet the two kinds of words are also semantically distinct in
many respects (e.g. dynamicity, causation, the range of
semantic fields, and the degree of semantic specificity),
and these differences in content may be correlated with
differences in neural substrates, such as the relevance of
the motion-related posterior middle temporal region for action
verbs but not for locative prepositions.
The neurocognitive differences between the meanings of
action verbs and locative prepositions lead to the prediction
that these two types of words could, at least in principle, be
impaired independently of each other as a result of focal brain
damage. This prediction was confirmed in two neurological
patients who exhibited a double dissociation in their performance on two large batteries of tests, one focusing on multiple
ways of processing the meanings of action verbs and the other
focusing on multiple ways of processing the meanings of
locative prepositions.
Subjects
Subject 1
JP is a fully right-handed (þ100 on the Geschwind-Oldfield
scale) man who obtained a college education and worked as a
drug store owner and operator until retiring around age 70. In
1987, at age 76, he suffered a left hemisphere infarction,
which produced a severe aphasia and a mild right hemiparesis.
On initial evaluation in the Benton Neuropsychology Laboratory conducted 10 days post-onset, JP demonstrated a severe
non-fluent aphasia, most closely resembling a Broca-type,
but he no longer had any hemiparesis, and his non-verbal
abilities, including paralinguistic communication, were wellpreserved. We have studied JP on a regular basis ever since
the onset of his condition. He has continued to manifest a
severe expressive language impairment, which can be classified as a Broca-type aphasia, but his general cognitive abilities
are otherwise well preserved. He is fully cooperative with all
neuropsychological procedures, and he is readily capable of
grasping task instructions provided they are given slowly with
non-verbal accompaniments. In fact, he has excellent verbal
comprehension in conversational speech formats, even though
his performances on formal tests of aural comprehension tend
to be impaired (see Table 1). Also, JP remains capable of
singing very well.
JP’s lesion is depicted in Fig. 1, which shows a threedimensional reconstruction with Brainvox (Frank et al., 1997)
based on an MRI scan conducted 6/25/99.
The lesion is in the heart of Broca’s area, in the left frontal
operculum. The pars opercularis and pars triangularis are
damaged, along with the underlying white matter. Cortically,
the lesion extends anteriorly into the ventrolateral prefrontal
region, in the pars orbitalis, and superiorly into the middle
part of the premotor region (area 6). The anterior insula is
damaged. However, the precentral gyrus and basal ganglia are
minimally affected, which could explain why JP demonstrated virtually no right-sided motor defect. Posteriorly, there
is no significant cortical involvement past the Rolandic sulcus; however, some of the white matter underneath the postcentral gyrus and inferior parietal lobule is affected. The
temporal lobe appears to be entirely spared.
Table 1 shows JP’s performance on standardized neuropsychological tests that are commonly used in the Benton
Neuropsychology Laboratory and that give a comprehensive
overview of his mental capacities (Tranel, 1996).
These data were collected between 1999 and 2000, contemporaneously with the lesion data and with the experimental studies reported below. JP performed primarily within the
average range on various subtests of the WAIS-III and the
WRAT-III. His score on a test of non-verbal anterograde
memory was normal. (The patient’s aphasia precluded valid
administration of verbal IQ and memory tests.) Regarding his
linguistic abilities, many subtests from the Multilingual
Aphasia Examination and the Boston Diagnostic Aphasia
Examination were administered, and he was impaired on
all of them except for the two basic reading measures. His
ability to comprehend written words was fairly wellpreserved, but his reading speed was defective.
JP was also given several tests that evaluate visual object
recognition and spoken naming across different conceptual
categories (Tranel et al., 1997). The stimuli consisted of line
drawings of objects, and accurate naming responses were
accepted as correct identification. If naming was inaccurate or
absent, the subject was prompted to generate specific, detailed
descriptions of the stimuli. These were rated by experimenters
to determine whether they conveyed sufficient information
Double dissociation between verbs and prepositions
425
Table 1. Comprehensive neuropsychological evaluations of JP and RR
JP
Intellect and academic achievement
Wechsler Adult Intelligence Scale-III (Scaled scores)
Performance IQ
Picture Completion
Digit symbol-coding
Block design
Matrix reasoning
Picture arrangement
Wide range achievement test-III (Standard scores)
Reading
Non-verbal anterograde memory
Benton visual retention test (correct/errors)
Standardized assessment of language
Multilingual aphasia examination (Percentiles)
Controlled oral word association
Visual naming
Sentence repetition
Token test
Aural comprehension
Reading comprehension
Boston diagnostic aphasia examination
Boston naming (#/60)
Responsive naming (#/30)
Reading (#/10)
Iowa-Chapman speed of reading (#/25)
Visual object recognition and spoken naming
Animals (n ¼ 41)
Recognition
Naming (for the items correctly recognized)
Fruits/Vegetables (n ¼ 32)
Recognition
Naming (for the items correctly recognized)
Tools/Utensils (n ¼ 63)
Recognition
Naming (for the items correctly recognized)
Vehicles (n ¼ 12)
Recognition
Naming (for the items correctly recognized)
Musical instruments (n ¼ 12)
Recognition
Naming (for the items correctly recognized)
RR
Score
Interpretation
Score
Interpretation
100
9
7
12
11
12
Average
Average
Low average
High average
average
High average
132
16
10
12
17
17
Superior
Superior
Superior
High average
Superior
Superior
93
Average
68
Borderline
6/6
Normal
8/3
Normal
<1st %ile
<1st %ile
<1st %ile
<1st %ile
<1st %ile
59th %ile
Defective
Defective
Defective
Defective
Defective
Normal
<1st %ile
<1st %ile
<1st %ile
<1st %ile
<1st %ile
59th %ile
Defective
Defective
Defective
Defective
Defective
Normal
12
24
7
4
Defective
Defective
Borderline
Defective
9
6
9
10
Defective
Defective
Normal
Defective
59% (z ¼ 11.8)
50% (z ¼ 14.7)
Defective
Defective
88% (z ¼ 1.4)
44% (z ¼ 16.7)
Normal
Defective
81% (z ¼ 3.0)
31% (17.1)
Defective
Defective
97% (z ¼ 1.1)
65% (z ¼ 7.9)
Normal
Defective
97% (z ¼ 0.2)
61% (9.3)
Normal
Defective
98% (z ¼ 0.5)
29% (z ¼ 18.0)
Normal
Defective
100% (z ¼ 0.8)
92% (z ¼ 2.7)
Normal
Defective
100% (z ¼ 0.8)
58% (z ¼ 19.7)
Normal
Defective
Defective
Defective
100% (z ¼ 1.1)
25% (z ¼ 16.0)
Normal
Defective
99th %ile
40th %ile
31
29
High normal
Normal
Normal
Normal
83% (z ¼ 3.9)
40% (z ¼ 12.6)
Visuospatial perception/construction
Facial discrimination
Judgment of line orientation
Complex figure copy (#/36)
Three-dimensional block construction (#/29)
32nd %ile
74th %ile
32
29
Normal
High normal
Normal
Normal
Executive function
Wisconsin card sorting test
Categories completed
Perseverative errors
6
16
Normal
Normal
about the entity to support the scoring of the response as a
correct identification, i.e. as adequate retrieval of conceptual
knowledge. JP’s recognition was normal for the categories of
tools/utensils and vehicles, but was impaired for the categories of animals, fruits/vegetables, and musical instruments.
His naming was impaired for all of the categories.
Turning to the assessment of visuospatial perception and
construction, JP performed well on all of the tests that were
administered. Finally, with regard to executive functions, it is
6
7
Normal
Normal
notable that he performed well on the Wisconsin Card Sorting
Test, indicating preservation of higher-order reasoning and
judgment capacities.
Subject 2
RR is a fully right-handed (þ100) man who obtained a
master’s degree in international affairs and worked for
roughly 40 years in the printing and publishing business.
426
D. Kemmerer and D. Tranel
Fig. 1. Lesion reconstruction for patient JP from a magnetic resonance
imaging scan.
The damage affects most of the cortex and white matter in
the supramarginal and angular gyri, and the posterior part of
the superior temporal gyrus; i.e. nearly all of what is usually
demarcated as Wernicke’s area. There is an additional, smaller area of damage in the left prefrontal region, in the pars
opercularis, as well as some damage in the white matter of the
left temporal pole. Both the cortex and underlying white
matter associated with the middle temporal gyrus, including
the posterior extension of this region into the temporo-occipital transition zone, are undamaged. Initially he displayed
global aphasia, but this gradually resolved. In fact, by the time
he initially came to our laboratory in 1995, his general
communication abilities were remarkably effective, even
though his performance on formal language tests remained
for the most part impaired, as described below.
The results of RR’s general neuropsychological assessment
are shown in Table 1. These data were obtained contemporaneously with both the lesion data and the experimental
studies reported below. His performance IQ was well above
average (132), and he obtained superior scores on many of the
subtests of the WAIS-III. On the WRAT-III, however, he had
borderline reading performance. His score on a test of
non-verbal anterograde memory was normal. (As with JP,
the patient’s aphasia precluded valid administration of verbal
IQ and memory tests.) Regarding linguistic abilities, like JP
he was impaired on all of the aphasia subtests except for the
two basic reading measures. Also like JP, while his written
comprehension was intact, his reading speed was poor. With
respect to visual object recognition and spoken naming, RR
exhibited a consistent pattern of normal recognition but
impaired naming for all of the categories that were tested.
It is noteworthy, however, that separate experiments revealed
intact written naming for all of the categories (mean ¼ 92%,
s.d. ¼ 6.5%; see Kemmerer et al., submitted). This constitutes
further evidence that his conceptual knowledge of concrete
entities is normal, and also indicates that his poor spoken
naming is probably due to a deficit at one or more of the stages
along the processing pathway that leads from meaning to
articulation. Shifting to the domain of visuospatial perception/
construction, his scores were uniformly in the normal to highnormal range. Finally, his executive functions were wellpreserved, as indicated by normal performance on the
Wisconsin Card Sorting Test.
Experiments Involving action verbs
Methods
Fig. 2. Lesion reconstruction for patient RR from a magnetic resonance
imaging scan.
In January, 1991, at the age of 62, he suffered a left hemisphere infarction. The patient’s lesion is depicted in Fig. 2,
which shows a three-dimensional reconstruction with Brainvox based on an MRI scan conducted 7/13/00.
Six tests were used to evaluate the subjects’ ability to produce,
comprehend, and semantically analyze action verbs. The
design characteristics and processing requirements of the
tests are described below. A complete list of the items used
in the tests is provided by Kemmerer et al. (2001a), and
further details appear in Fiez and Tranel (1997). [Some of the
original tests described by Fiez and Tranel (1997) had a few
more items than were used in the study by Kemmerer et al.
Double dissociation between verbs and prepositions
(2001a). Some items were omitted because of unreliable
performances in normal control subjects. The slightly modified tests presented in Kemmerer et al. (2001a) are the same
ones that were employed in the current study].
Naming test
100 color photographs of various actions are presented to the
subject on a Caramate 4000 slide projector in free field. Each
picture is intended to elicit a specific verb or else one of a
small set of verbs that are all considered to be acceptable
responses based on normative data. The first 75 items are
single pictures that show ongoing activities (e.g. swimming),
and the last 25 items are picture pairs that show both the initial
and final states of completed events (e.g. peeled). The target
verbs in this test (and also in the other tests) come from a wide
range of semantic fields. The test requires recognizing the
objects in the pictures as well as inferring what kind of action
is taking place, i.e. activating the most appropriate action
concept. Once an action concept has been activated, the verb
semantic structure that corresponds most closely to it is
selected, and then the verb’s phonological form is retrieved
for production.
Verb-picture matching test
For each item, a written verb is presented to the subject
together with color photographs of two different actions,
and the subject’s task is to determine which action the verb
describes. For example, in one item the verb is kicking and the
two pictures show a person kicking a ball and a person rolling
a ball. There are 69 items. The first 43 items contain single
pictures of ongoing activities, and the last 26 contain picture
pairs showing the initial and final states of completed events.
Like the Naming test, this test requires complex visual
processing of the pictorial stimuli; however, while the Naming
test only has one picture (or picture pair) per item, the
Matching test has two, so the visual processing demands
are greater. On the other hand, although both the Naming
test and the Matching test require activating the semantic
structures of verbs, only the Naming test also requires voluntary retrieval of the phonological forms of verbs, so in this
regard the Matching test may be somewhat easier than the
Naming test.
Picture attribute test and word attribute test
The next two tests are similar insofar as they both emphasize a
certain kind of analytic or inferential processing, specifically
the ability to compare the values of two action concepts for a
particular predetermined attribute. In the Picture Attribute
test, the subject is shown two color photographs of actions (or
two pairs of them) arranged on pages in a binder notebook,
and is asked a question about which action satisfies a particular value for a single attribute. The test contains 72 items, 48
of which have single pictures of ongoing actions and 24 of
which have picture pairs for completed events. The attribute
questions are as follows: (1) Which action makes the loudest
noise? (2) Which action would be most physically tiring? (3)
427
Which action would take more time to complete? (4) Which
action would require a specified kind of movement (e.g.
moving hands closer together, moving hands up/down, moving hands in a circle)? (5) Which action would be most
enjoyable/harmful/helpful? (6) Which change of state was
accomplished using a particular tool or utensil (e.g. knife,
hammer)? (7) Which change of state was most permanent? (8)
Which change of state best represented an improvement to the
object? This test requires visual processing of the pictorial
stimuli and activation of the appropriate action concepts. The
main task of answering the attribute questions involves the
following additional operations: decomposing the internal
structure of each action concept, identifying the attribute at
issue, determining its typical value, comparing the values for
the different concepts, and making a decision about which one
fulfills the target criterion. This test does not explicitly involve
verbs in either the stimuli or the responses; nevertheless, it is
likely that normal subjects make use of verbs when they
perform the test, especially given the larger situational context
of taking a series of tests that probe knowledge of verbs (see
Gennari et al., 2002, for related experiments and discussion).
The Word Attribute test is parallel in design to the Picture
Attribute test, except the stimuli are written verbs instead of
pictures. There are 62 items, 40 with verbs in progressive form
and 22 with verbs in past tense form. With respect to
processing requirements, the semantic structures of the verbs
must be activated, and we assume that it is through these
language-specific representations that more richly detailed
action concepts are retrieved. Real-world knowledge about
typical action scenarios is necessary in order to answer the
attribute questions for many of the items. For instance, in one
item the two verbs are singing and yawning, and the attribute
question is which action makes the loudest sound. Although
the answer is clearly singing, this reflects knowledge about
how the two actions are typically executed, not how they are
necessarily executed; after all, it is obviously possible for
someone to sing very softly or yawn very loudly.
Picture comparison test and word comparison test
The last two tests are similar to the previous two tests in that
they emphasize analytic/inferential processing, but they are
unique in the specific nature of these processing requirements.
In particular, both of these tests employ an ‘‘odd one out’’
paradigm in which the subject must compare three verb
meanings and identify the one that is unrelated to the other
two; moreover, the relevant criteria for comparison are not
provided by the experimenter but must be discovered by the
subject.
The Picture Comparison test has 24 items, and each item
consists of three photographs of ongoing actions arranged on
pages in a binder notebook. The subject’s task, as alluded to
above, is to indicate which picture shows a type of action that
is somehow different from the other two. For example, in one
item the three pictures show (1) a person wrapping a box with
paper, (2) a person wrapping her wrist with a cloth, and (3) a
person drying a plate with a towel. The visual processing
428
D. Kemmerer and D. Tranel
demands for this test are substantial because three different
pictures must be studied. In addition, a great deal of conceptual processing is required in order to determine which
aspects of the depicted actions are most relevant for sorting
them. As in the Picture Attribute Test, although verbs are not
explicitly employed in either the stimuli or the responses, it is
reasonable to assume that normal subjects sometimes use an
implicit naming strategy to facilitate performance (again, see
Gennari et al., 2002, for related experiments and discussion).
Moreover, some of the items may depend on idiosyncratic
aspects of the semantic structures of English verbs
(Kemmerer et al., 2001a).
The Word Comparison test is parallel in design to the
Picture Comparison test, except the stimuli for each item
consist of three verbs instead of three pictures. There are 44
items, and the subject’s task is to indicate which verb is
somehow different in meaning from the other two. In each
item, the two associated verbs have one of four types of
semantic relation: synonymy, antonymy, hyponymy, and
cohyponymy. In order to identify the appropriate relational
dimension for grouping the verbs, the subject must retrieve
and analyze the relevant semantic structures. As in the Word
Attribute test, performance may be enhanced by also generating and inspecting mental images of particular action
scenarios, since this could facilitate recognition of the features
that are most important for the comparison process.
Results and discussion
JP’s and RR’s performances were evaluated relative to the
following control data from Fiez and Tranel (1997):
Naming (mean ¼ 85.0%, s.d. ¼ 5.0); Verb-Picture Matching
(mean ¼ 92.1%, s.d. ¼ 4.6); Picture Attribute (mean ¼ 91.7%,
s.d. ¼ 4.8); Word Attribute (mean ¼ 94.8%, s.d. ¼ 3.6); Picture
Comparison (mean ¼ 83.6%, s.d. ¼ 8.3); Word Comparison
(mean ¼ 88.7%, s.d. ¼ 8.1). [As noted earlier, some of the
original tests described by Fiez and Tranel (1997) had a few
more items than were used in the current study. The control data
shown above reflect these adjustments.] For each test, a percent
correct was calculated, and this was then converted to a z-score.
Following standard convention, a subject was classified as
impaired on a given test if the z-score was equal to or lower
than -2.0 (see Damasio et al., in press).
The results are presented in Table 2.
Table 2. Results for tests involving action verbs
JP
Naming
Matching
Picture attribute
Word attribute
Picture comparison
Word comparison
RR
%
z
%
z
33
72
82
79
25
59
10.4
4.3
2.0
4.4
7.1
3.4
22
99
89
94
58
64
12.6
1.4
0.6
0.3
3.0
2.9
JP failed all six tests. His performance was extremely poor
on both the Naming test and the Picture Comparison test, and
his scores were also far below normal for the Verb-Picture
Matching test, the Word Attribute test, and the Word Comparison test. His best performance was on the Picture Attribute
test, but even here his score was still at the cutoff point for
impairment. RR, on the other hand, exhibited a mixed pattern
of performance across the six tests. He was impaired on the
Naming test and also failed both of the Comparison tests, but
he was nearly perfect on the Verb-Picture Matching test and
was normal on both of the Attribute tests. Another way of
portraying the differences between JP’s and RR’s performances is by directly comparing their scores. If we exclude
the Naming test (on which both patients were severely
impaired) and compute average scores for each patient on
the remaining tests, it becomes clear that RR’s performance
was much better than JP’s: RR’s mean percent correct was
80.8 whereas JP’s was 63.4, a difference of 17.4 points; and
RR’s mean z-score was 1.08 (which is well within the
normal range) whereas JP’s was 4.24 (which is well into
the defective range), a difference of 3.16 points. Moreover,
RR’s scores were consistently higher than JP’s on every test
except Naming, which further accentuates RR’s superior
performance relative to JP’s. In what follows, we look more
closely at each patient’s performance profile, focusing first on
JP and then shifting to RR.
As noted in the earlier discussion of JP’s overall neuropsychological assessment, he has normal recognition of tools/
utensils and vehicles but impaired recognition of animals,
fruits/vegetables, and musical instruments (Table 1). It is
unlikely, however, that his category-related object recognition
deficits contributed significantly to his failure on the tests of
action verbs. Two of the tests – Word Attribute and Word
Comparison – use only linguistic stimuli and hence do not
require visual object recognition at all, yet JP still performed
quite poorly. Moreover, even though the other four tests
employ pictures as stimuli, only a very small number of items
include objects from the categories that are challenging for JP;
instead, the vast majority of items have people and tools/
utensils as the most important entities in the actions, and JP
has normal recognition of these kinds of entities. These
considerations suggest that JP’s low scores on the six tests
stem from problems with verb processing rather than from
category-related object recognition deficits.
In the Methods section, we pointed out that the six tests are
designed to measure verb knowledge from many different
angles. In a previous study with a group of 89 neurological
patients, we found that 30 of the patients were impaired on at
least one of the tests and that they manifested a total of 22
distinct performance profiles, with each test dissociating from
all of the others – a finding which constitutes experimental
evidence that the tests do in fact require different processing
operations that can be disrupted independently of each other
(Kemmerer et al., 2001a, b). Regarding JP’s performance
profile, it may be that he has a combination of impairments
affecting several different aspects of verb processing. However,
Double dissociation between verbs and prepositions
given that he failed the entire set of tests, the simplest explanation is that, at the very least, he has a representational disorder
affecting his knowledge of the semantic structures encoded by
action verbs.
Turning now to RR, as noted earlier he failed three of the
tests (Naming, Picture Comparison, and Word Comparison)
but passed the others (Verb-Picture Matching, Picture Attribute, and Word Attribute). This pattern suggests that his
knowledge of verb meanings is still mostly intact, because
otherwise he would not have been able to achieve such high
scores on half of the tests in the battery. Additional evidence
that he retains substantial knowledge of the semantic structures of action verbs comes from three other studies in which
he performed within normal limits on forced-choice threealternative verb-picture matching tasks (Kemmerer, 2000a,
2003; Kemmerer and Wright, 2002). [He is referred to as
1962RR in those studies. JP did not participate in the studies,
so we do not have data for him.] To fully account for RR’s
performance profile, however, it is necessary to explain why
he obtained low scores on certain tests. This is a complex
issue, and below we elaborate and evaluate several different
approaches to addressing it.
First, in the three studies mentioned above (Kemmerer,
2000a, 2003; Kemmerer and Wright, 2002), RR consistently
displayed robust dissociations between, on the one hand,
preserved sensitivity to subtle, idiosyncratic semantic features
of verbs that are irrelevant to grammar, and on the other hand,
impaired sensitivity to aspects of linguistic meaning that
strongly influence the interaction between verbs and various
morphosyntactic constructions (see also Kemmerer, 2000b,
for an analogous study involving prenominal adjective order).
It is important to consider whether these findings can shed any
light on RR’s performance profile in the current study. Space
limitations preclude a summary of all of the studies, but we
will attempt to convey a sense of the general pattern of results
by reviewing the essential elements of just one study, namely
the study that focused on the verbal un- prefixation construction (Kemmerer and Wright, 2002).
This construction is directly associated with the schematic
meaning ‘‘X causes Y to come out of a constricted spatial
configuration relative to Z’’, and hence it only licenses verbs
that express the creation of some kind of constricted spatial
configuration which is potentially reversible (e.g. wrapunwrap, buckle-unbuckle, clog-unclog versus press- unpress,
press, rotate- unrotate, submerge- unsubmerge). These
semantic constraints are revealed in a rather striking way
by the different uses of the verb cross: one can cross one’s
arms and then uncross them (because a constricted spatial
configuration is created and then reversed), but if one crosses a
street and then walks back again, it would sound strange to say
that one has uncrossed the street (because no constricted
spatial configuration is involved). RR performed well on a
verb-picture matching test that required him to discriminate
between aspects of verb meaning that are completely irrelevant to un-prefixation (e.g. he correctly selected twisting
instead of bending or folding to describe a picture of a woman
429
twisting a long thin sponge; note that all three verbs satisfy the
general semantic criteria for un-prefixation but differ in the
unique kinds of object manipulations that they encode).
However, he failed a grammaticality judgment test that
probed his knowledge of the particular semantic features that
determine which verbs can occur in the construction (e.g. he
incorrectly rated the verbs uncoil, unclip, and unshackle as
being ungrammatical, and incorrectly rated the verbs unturn,
undangle, and unfluff as being grammatical). A third test
showed that his failure on the judgment test was not due to
problems with various task demands, but was instead most
likely due to a disturbance of his knowledge of the semantic
constraints on un-prefixation.
These findings (and analogous findings in the other studies
cited above) suggest that RR has some kind of impairment of
grammatically relevant aspects of linguistic meaning. The
question at hand is whether this information can provide
insight into RR’s performance profile across the six verb tests
in the current study. While granting that the issues surrounding this question are quite complicated, we suspect that the
answer is no, for the following two reasons. First, all of the
tests in the verb battery depend far more on knowledge of
grammatically irrelevant aspects of verb meaning than on
grammatically relevant aspects, so there is no obvious reason
why an impairment of the latter would cause RR to fail any of
the tests, let alone just the Naming test and the two Comparison tests. Second, although it is possible that RR has an
impairment of the grammatically relevant aspects of verb
meanings, it is also possible that he does not. This is because
his failure on the various grammaticality judgment tests that
probe his sensitivity to the semantic factors underlying the
interaction between verbs and certain morphosyntactic constructions could in principle reflect an impairment that largely
spares verb meanings and instead affects constructional meanings (for elaboration of the distinction between verb meanings
and constructional meanings, see Goldberg, 1995, 2003).
[This uncertainty as to the exact nature of RR’s disorder of
grammatical semantics is discussed in the papers cited above
(Kemmerer, 2000a, p. 1014; Kemmerer and Wright, 2002,
p. 421; Kemmerer, 2003, p. 29).]
Another approach to explaining RR’s low scores on the
Naming test and on the two Comparison tests is based on the
fact that Fiez and Tranel’s (1997) control subjects performed
worse on these three tests (with means between 83.6% and
88.7% and standard deviations between 5.0 and 8.3) than on
the other three tests (with means between 91.7% and 94.8%
and standard deviations between 3.6 and 4.8), suggesting
differences in difficulty. Thus one might suppose that RR’s
deficits only become apparent on the more challenging tests in
the battery. An explanation along these lines could perhaps be
applied to RR’s failure on the two Comparison tests because
although his z-scores of 3.0 and 2.9 are plainly in the
defective range, they are not dramatically low. However, such
an explanation is less plausible for RR’s failure on the Naming
test because his z-score of 12.6 is far out of proportion to the
others.
430
D. Kemmerer and D. Tranel
Yet another approach, which is an extension of the previous
one and is our preferred interpretation of the data, is that RR
has several distinct impairments that interfere with specific
ways of processing the forms and meanings of verbs while
leaving the semantic structures themselves more or less intact.
Looking first at his failure on the two Comparison tests, this
could derive from a moderately impaired ability to carry out
one or more of the analytic operations that are shared by those
tests but are not required by any of the other tests, such as
identifying the particular semantic criteria that are relevant to
sorting the three stimuli in each item (Kemmerer et al.,
2001a). This approach to explaining RR’s performance is
admittedly speculative, but it is much more precise than
merely saying that the two Comparison tests are more ‘‘difficult’’ than the other tests. Regarding his failure on the Naming
test, it is most likely due to a deficit involving lexical access
and/or phonological planning. In our presentation of RR’s
neuropsychological background, we pointed out that he has
impaired spoken naming of various categories of concrete
entities but preserved written naming of the very same
entities. Given this context, it seems quite plausible that his
low score on the Naming test in the verb battery reflects a
disorder which affects the phonological production of not just
nouns but also verbs. We did not test RR’s written naming of
actions because at the time that the verb battery was administered, we had not yet systematically investigated his superior written over spoken naming of concrete entities; however,
we predict that his written naming of actions would be within
the normal range because, first, his knowledge of verb meanings appears to be mostly intact, and second, the available data
suggest that his word production deficit is restricted to the
phonological modality. This prediction is consistent with
documented cases of patients who have better written than
spoken production of verbs (e.g. Hillis and Caramazza, 1995;
Hillis et al., 2002a). Unfortunately, however, the prediction
cannot be tested because RR recently passed away.
Overall, the essential point that we would like to emphasize
is that even though RR is apparently deficient at processing
the semantic and phonological structures of verbs in certain
ways, his representational knowledge of verb meanings seems
to be fairly well-preserved. This certainly appears to be the
case for the grammatically irrelevant aspects of verb meanings, and it may also be true for the grammatically relevant
aspects, although the actual status of this component of verb
meanings remains ambiguous.
red arrow, and the landmark is indicated by a green arrow.
Based on normative data, each picture is associated with
either a single preposition or with two very similar prepositions (e.g. in back of and behind). The number of pictures for
each preposition is as follows: on (13), in (13), around (3),
through (3), above/over (13), below/under (13), in front of (6),
in back of/behind (6), beside/next to (6), and between (4). For
many of these prepositions, prototypical as well as nonprototypical situations are illustrated in the pictures.
Experiments involving locative prepositions
Odd one out test
The subject is shown 45 sets of three pictures, with each set
organized in the same manner as in the Matching #2 test. For
this test, though, the task is to determine which picture in each
set shows a spatial relationship that is different from the
others – a paradigm similar to the one used for the Picture
Comparison Test and the Word Comparison Test in the battery
for action verbs. The red and green arrows pointing to the
figure and landmark objects are crucial because without them
Methods
Five tests were used to evaluate the subjects’ knowledge and
processing of locative prepositions. The stimuli for the first
four tests consist of 80 black-and-white photographs of real
objects in various spatial relationships (for a complete
description of the items used in these tests, see Kemmerer
and Tranel, 2000a). In each picture the figure is indicated by a
Naming test
All 80 pictures are presented to the subject on a Caramate
4000 slide projector in free field. For each one, the subject is
asked a question designed to elicit the preposition that best
describes the depicted spatial relationship – e.g. ‘‘Where is the
cap in relation to the chair?’’ (answer ¼ on). The processing
operations required by the test include recognizing the objects
shown in each picture, categorizing their spatial relationship
according to the most appropriate prepositional semantic
structure, and retrieving the phonological form of the preposition so it can be articulated.
Matching #1 test
The same 80 pictures are presented again in the same manner,
only this time the subject is asked to choose which of three
written prepositions best describes each situation – e.g. ‘‘The
cap is in/on/beside the chair’’ (answer ¼ on). This test differs
from the Naming Test insofar as it requires comprehension
rather than production of prepositions. In addition, it has a
linguistic emphasis since it requires comparing the visuospatial representation of each picture with the semantic structures of three different prepositions, and then selecting the
best match.
Matching #2 test
The subject is shown 50 sets of three pictures, with each set
arranged on a separate page in a binder notebook. For a given
set, the task is to determine which picture best represents a
particular written preposition. Thus, for one item the preposition is in and the three pictures show (1) a window above
another window, (2) eggs in a carton, and (3) a boy on a swing.
This test differs from the Matching #1 Test insofar as the
emphasis here is more on visual than linguistic processing,
since the subject must compare the representations of three
different pictures with the semantic structure of a single
preposition and then select the best match.
Double dissociation between verbs and prepositions
the subject would not be constrained in determining which
objects, and hence which spatial relationships, to attend to.
However, the subject cannot rely on just the placement of the
arrows in performing the task but must focus on the objects
that the arrows pointed to. Many of the items in this test
require access to the crosslinguistically unique semantic
structures of English prepositions. For example, one item
has the following three pictures: (1) a design on the side of a
coffee cup, (2) a boy on a tricycle, and (3) eggs in a carton. In
order to determine that the first two pictures are similar
whereas the third is the ‘‘odd one out’’, the subject must
recognize that the first two pictures both represent spatial
relationships that involve contact but not containment,
whereas the third picture represents a spatial relationship that
involves both of these features, especially the latter. These are
the semantic features that distinguish on from in. If one did
not take them into account but instead relied solely on
nonlinguistic perceptual features to perform the task, it is
unlikely that one would be able to arrive at the correct answer
because there are so many perceptual dimensions along which
the pictures could be compared. For instance, one could treat
the first picture as the ‘‘odd one out’’ because it represents a
spatial relationship in which the figure is literally part of the
landmark, whereas the second and third pictures represent
spatial relationships in which the figure and landmark are
independently moveable objects.
Verification test
This test employs a different set of visual stimuli than the first
four tests. The subject is shown 44 line drawings of abstract
shapes in various spatial relationships. In each picture, one
shape is dark and the other light. The subject’s task is to
determine whether the meaning of a particular written preposition correctly describes the location of the dark object
relative to the light one. The number of pictures representing
each preposition is as follows: on (6), in (6), around (4),
across (4), above/over (6), below/under (6), next to/beside (6),
and between (6). Since the shapes do not represent real
objects, the visual processing of object-internal features is
minimized while that of inter-object spatial relationships is
maximized.
Results and discussion
JP’s and RR’s performances were evaluated relative to a
control group of 10 neurologically and psychiatrically
healthy subjects with the following demographic characteristics: male/female gender ratio (5/5); age (mean ¼ 50.2,
s.d. ¼ 8.6); education (mean ¼ 13.6, s.d. ¼ 2.2); handedness
(all right-handed). The control subjects performed well on all
of the tests: Naming (mean ¼ 91.0%, s.d. ¼ 4.6); Matching #1
(mean ¼ 92.4%, s.d. ¼ 4.1); Matching #2 (mean ¼ 97.6%,
s.d. ¼ 2.3); Odd One Out (mean ¼ 94.7%, s.d. ¼ 3.6); Verification (mean ¼ 91.0%, s.d. ¼ 4.3). JP’s and RR’s data were
analyzed by first calculating the percent correct for each test,
and then converting the percentage scores to z-scores. As with
431
Table 3. Results for tests involving locative prepositions
JP
Naming
Matching #1
Matching #2
Odd one out
Verification
RR
%
z
%
z
93
94
100
100
–
.4
.4
1.0
1.5
–
68
70
74
62
72
5.0
5.5
10.3
9.1
4.4
the tests for action verbs, the cutoff for impairment on each
test was set at a z-score of 2.0. The results are shown in
Table 3.
JP performed extremely well on the Naming test, the two
Matching tests, and the Odd One Out test. We were unable to
administer the Verification test to him because it was not
available during the experimental session, but it is likely that
he would have passed it without difficulty since the extant data
indicate unambiguously that his knowledge of the meanings
of locative prepositions is fully intact.
In contrast, RR failed all of the tests, consistently obtaining
scores that were many standard deviations below the mean for
the control subjects. This outcome strongly suggests that his
knowledge of the meanings of locative prepositions is disrupted. This view is further supported by an analysis of the
distribution of his errors, as shown in Table 4. The results
clearly indicate that he was impaired on geometrical as well as
projective prepositions in all of the different testing formats.
Thus the disruption of his knowledge of the semantic structures encoded by locative prepositions appears to be quite
broad.
It is possible that RR’s failure on the Naming test was
exacerbated by difficulty retrieving the phonological forms of
prepositions. This hypothesis derives from data and arguments presented earlier which suggest that he has a spoken
word production deficit for both nouns and verbs. It is also
important to note, however, that RR’s failure on the other tests
is probably not due to an impairment of just the forms, as
opposed to the meanings, of prepositions. In both of the
Matching tests as well as in the Verification test, prepositions
are presented in written format (and are also read aloud by the
experimenter), and RR’s orthographic input lexicon appears
to be intact, based on his good performance on standardized
reading tests (Table 1). Furthermore, although the Odd One
Out test depends on knowledge of the language-specific
semantic structures of prepositions, it does not require overt
processing of the forms of prepositions in either the stimuli or
the responses.
Another important point about RR’s performance profile is
that there is no evidence that his failure on the entire battery of
preposition tests might reflect some kind of non-linguistic
deficit involving the perceptual processing of the visuospatial
stimuli. Independent testing demonstrated that his object
recognition abilities are normal (Table 1), and anyhow the
432
D. Kemmerer and D. Tranel
Table 4. Distribution of RR’s errors in the tests involving locative prepositions. Cells indicate the number (and percentage) of items that were answered correctly
out of the total possible
Preposition
Naming
on
in
around
through
across
above/over
below/under
in front of
in back of
beside
between
9/13
9/13
1/3
1/3
8/13
10/13
4/6
5/6
5/6
2/4
8/13
10/13
2/3
2/3
–
7/13
12/13
4/6
6/6
4/6
2/4
Total
54/80 (68%)
56/80 (70%)
–
Matching #1
Matching #2
Odd one out
3/8
6/8
3/3
0/3
8/10
7/10
1/2
0/2
–
Verification
5/6
3/6
3/4
–
–
8/8
7/8
3/4
4/4
3/4
3/6
4/6
2/3
1/3
2/3
–
–
37/50 (74%)
28/45 (62%)
Verification test does not even require object recognition.
Furthermore, independent testing demonstrated that his
visuospatial processing abilities are also normal (Table 1).
This is especially significant in the present context because
two of the visuospatial tests – specifically, Complex Figure
Copy and Three-Dimensional Block Construction – assess
nonlinguistic processing of the same general kinds of categorical spatial relationships that are encoded by prepositions.
As we mentioned in the Introduction, however, the meanings
of prepositions may be representationally autonomous, one
reason being that there are substantial crosslinguistic differences in the particular categorical spatial distinctions made by
prepositions, which suggests that when people talk about the
spatial world, they must package their experience in ways that
reflect the unique perspective captured by the inventory of
prepositions in the given language. The notion that the
semantic structures of prepositions are independent,
language-specific mental representations is supported by
RR’s dissociation between, on the one hand, impaired processing of categorical spatial relationships that are encoded by
prepositions, and on the other hand, intact processing of
categorical spatial relationships that are not encoded by
prepositions but are instead used for non-linguistic perceptual
and constructional tasks. The same type of dissociation, as
well as the opposite type of dissociation, was found in other
brain-damaged patients described by Kemmerer and Tranel
(2000a). The implications of this double dissociation are
discussed in depth in that paper (see also Kemmerer, submitted, for another case similar to RR).
General discussion
The two patients described in this study manifested opposite
patterns of performance on test batteries that evaluated production, comprehension, and semantic analysis of action verbs on
the one hand and locative prepositions on the other. Because the
combined results constitute a double dissociation, it is impossible to account for the patients’ differential performance in
terms of differential difficulty of the test batteries. Instead, the
2/4
4/6
5/6
–
–
6/6
4/6
Total
33/50
35/50
10/15
3/11
2/4
30/46
38/46
13/19
16/19
20/25
8/14
(66%)
(70%)
(75%)
(27%)
(50%)
(65%)
(83%)
(68%)
(84%)
(80%)
(57%)
32/44 (72%)
double dissociation is a powerful indicator that the meanings of
action verbs and locative prepositions involve distinct mental
representations and/or computations that can be independently
disrupted by brain damage.
JP failed the entire set of tests for verbs but performed
extremely well on the tests for prepositions. This robust
dissociation can be explained in terms of a representational
disorder that affects his knowledge of the meanings of action
verbs but spares his knowledge of the meanings of locative
prepositions. In contrast, RR exhibited the reverse dissociation, with worse performance on prepositions than on verbs.
His scores for the preposition tests were consistently in the
defective range, and his errors extended to all of the prepositions that were used, suggesting that his knowledge of the
meanings of these words is severely disrupted. However, he
performed remarkably well on three of the tests in the verb
battery, and he could only have gotten such high scores if his
knowledge of the meanings of action verbs were mostly intact.
He failed the remaining tests in the verb battery, but we argued
that the most plausible explanation of his low scores on those
tests is that they reflect impairments of specific processing
operations, such as discovering the appropriate semantic
criteria for sorting the stimuli (which is required by the
two Comparison tests) and accessing the phonological forms
of verbs (which is required by the Naming Test).
As indicated in the Introduction, action verbs and locative
prepositions differ along several conceptual parameters.
Action verbs encode dynamic events; many of them refer
to complex causal sequences; they are organized into
hundreds of classes and subclasses, each devoted to characterizing a particular semantic field; and they often specify
remarkably precise, fine-grained nuances of meaning. Locative prepositions, on the other hand, designate static situations; they never imply causation; they constitute a small
inventory of words with very little internal organization into
classes and subclasses; and the meanings that they express are
distinctive for being quite schematic and coarse-grained. The
discovery that these two categories of words dissociate from
each other in brain-damaged patients is therefore in accord
Double dissociation between verbs and prepositions
with the increasingly well-supported notion that lexicosemantic structures with different conceptual properties tend to have
different neural substrates (see reviews by Forde and
Humphreys, 2002; Martin and Chao, 2001).
JP and RR exhibited not only a linguistic double dissociation, but also to a large extent a corresponding neuroanatomical double dissociation. JP’s lesion is mostly restricted to
the left inferior and middle premotor/prefrontal region, and
this is one of the major areas to have been associated with the
meanings of action verbs (McCarthy and Warrington, 1985;
Daniele et al., 1994; Bak et al., 2001; Pulvermuller et al.,
2001; Tranel et al., in press). The correlation between JP’s
verb deficit and his premotor/prefrontal lesion provides
further evidence for the ‘‘direct matching hypothesis’’, which
holds that ‘‘we understand actions when we map the visual
representation of the observed action onto our motor representation of the same action’’ (Rizzolatti et al., 2001, p. 664;
see also Damasio, 1989; Stamenov and Gallese, 2002).
RR’s lesion, on the other hand, is primarily in the left
inferior parietal lobe and the left posterior superior temporal
region; most importantly, his lesion is centered in the supramarginal gyrus, which has been associated with the meanings
of locative prepositions (Kemmerer and Tranel, 2000a;
Damasio et al., 2001; Kemmerer, submitted; Tranel and
Kemmerer, submitted). As noted earlier, the middle temporal
gyrus, including its extension posteriorly into the temporooccipital transition zone, is not damaged.
These aspects of the relevant brain-behavior relationships
are fairly clear, but other aspects are more subtle. Although
RR’s lesion is concentrated in specific sectors of the left
parietal and temporal lobes, he also has a small amount of
damage in the left frontal operculum. It is apparently not large
enough to severely disrupt his knowledge of the meanings of
action verbs, but it may partially explain why he failed the
Naming test as well as the two Comparison tests in the verb
battery. Regarding the Naming test, the left frontal operculum
(especially the underlying white matter) may contribute to
retrieving the phonological forms of verbs (Tranel et al.,
2001; Hillis et al., 2002b), so it is possible that RR’s lesion
impaired this retrieval process. As for the two Comparison
tests, several recent studies have implicated the left inferior
prefrontal cortex (especially Brodmann’s areas 44 and 47) in
various kinds of semantic working memory tasks that involve
accessing, maintaining, monitoring and manipulating semantic representations stored elsewhere (e.g. Poldrack et al.,
1999; Thompson-Schill et al., 1999; Devlin et al., 2003).
Perhaps this region subserves certain semantic computations
that are necessary for the Comparison tests but not for any of
the tests that RR passed. A problem with this account,
however, is that many of the patients in the group study
reported by Kemmerer et al. (2001a) had damage in the left
inferior prefrontal cortex but nevertheless performed within
normal limits on one or both of the Comparison tests. And
more generally, the fact that the 30 patients described in that
study exhibited 22 distinct performance profiles across the six
tests in the verb battery suggests that each test has certain
433
unique processing requirements that can be independently
impaired, which in turn implies that the neural basis of
semantic working memory is probably quite complex. More
research is clearly needed to explore this topic further.
Finally, it is interesting that neither patient has damage to
the region known as MT, which generally is thought to include
the transition zone between the posterior-most aspect of the
middle temporal gyrus and the bordering occipital cortex (e.g.
Dumoulin et al., 2000). This region has been associated with
action verbs, specifically the component of meaning that
involves visual motion patterns (Wise et al., 1991; Martin
et al., 1995; Fiez et al., 1996; Warburton et al., 1996; Kable
et al., 2002; Tranel et al., in press). If the findings of the
present study are integrated with the accumulating research on
area MT, the picture that emerges is one in which this area
(and the area just anterior and dorsal to it; see Kable et al.,
2002) plays an important but not sufficient role in the anatomically distributed neural system underlying verb semantics.
In particular, RR’s fairly well-preserved knowledge of action
verbs may be supported by a close interaction between area
MT and the left premotor/prefrontal cortex (most of which is
still intact for him, as discussed above); yet for JP, a fully
functioning area MT is apparently not enough to sustain
knowledge of action verbs when there is extensive damage
to the left premotor/prefrontal cortex (which is consistent with
the ‘‘direct matching hypothesis’’ mentioned earlier). The
intricacies of this neural circuitry will undoubtedly become
clearer as more research is done.
Acknowledgement
This work was supported by NINDS Program Project Grant
NS19632.
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435
A double dissociation between
the meanings of action verbs
and locative prepositions
David Kemmerer and Daniel Tranel
Abstract
We describe two patients who manifested opposite patterns of performance on
test batteries that evaluated production, comprehension, and semantic analysis
of action verbs on the one hand (e.g., smile, wave, run) and locative prepositions
on the other (e.g., in, on, over). JP failed all of the verb tests but passed all of the
preposition tests, suggesting impaired knowledge of the meanings of action
verbs but intact knowledge of the meanings of locative prepositions. In contrast,
RR exhibited the reverse dissociation: he passed many of the verb tests but
failed all of the preposition tests, suggesting mostly intact knowledge of the
meanings of action verbs but impaired knowledge of the meanings of locative
prepositions. This behavioral double dissociation reflects the fact that the two
categories of words differ along several conceptual parameters. To a large
extent, the patients exhibited a neuroanatomical double dissociation as well,
since JP’s lesion is predominantly in the left frontal operculum whereas RR’s is
predominantly in the left inferior parietal lobe and the posterior superior
temporal region. This constitutes preliminary evidence that the meanings of
action verbs and locative prepositions are represented by partially independent
neural networks in the brain.
Journal
Neurocase 2003; 9: 421–435
Neurocase Reference Number
564/02
Primary diagnosis of interest
Semantic impairments
Author’s designation of case
JP, RR
Key theoretical issue
* Neural and cognitive organization of different categories of word meanings
Key words: semantic structure; semantic memory; conceptual knowledge;
category specificity; verbs; prepositions
Scan, EEG and related measures
MRI
Standardized assessment
Western Adult Intelligence Scale (WAIS)-III, Benton Visual Retention Test
(BVRT), Multilingual Aphasia Examination, Boston Diagnostic Aphasia
Examination (BDAE). facial discrimination, judgment of line orientation,
Rey-Osterrieth Complex Figure, three-dimensional block construction, visual
object recognition and naming
Other assessment
Naming, matching, odd one out, and verification tests for verbs and prepositions
Lesion location
* JP: left frontal (pars opercularis, pars triangularis, pars orbitalis, and middle
premotor region, along with the white matter underlying these cortices); left
anterior insula; white matter beneath left postcentral gyrus and inferior
parietal lobule
* RR: cortex and white matter of left supramarginal, angular, and posterior
superior temporal gyri; pars opercularis of left frontal lobe; white matter of
left temporal pole
Lesion type
Cerebrovascular accident (stroke)
Language
English