Cognitive Brain Research 17 (2003) 484–494
www.elsevier.com / locate / cogbrainres
Research report
Category-specific medial temporal lobe activation and the
consolidation of semantic memory: evidence from fMRI
John Kounios a , *, Phyllis Koenig b , Guila Glosser b , Chris DeVita b , Kari Dennis b ,
Peachie Moore b , Murray Grossman b
a
b
Department of Psychology, Drexel University MS626, 245 North 15 th Street, Philadelphia, PA 19102 -1192, USA
Department of Neurology-2 Gibson, Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA 18194 -4283, USA
Accepted 29 April 2003
Abstract
Semantic memory consolidation was studied by comparing medial temporal lobe (MTL) fMRI activation to ANIMAL, IMPLEMENT
and ABSTRACT nouns in healthy seniors to that of young adults. Relative to healthy seniors, young adults were predicted to show greater
MTL activation for IMPLEMENTS, but not ANIMALS, because the ANIMALS category consists of highly intercorrelated and
overlapping features that should require less MTL-mediated binding than IMPLEMENTS over a shorter period of time during concept
consolidation. ABSTRACT meanings are context-dependent and do not consist of fixed feature sets. Thus it was predicted that
ABSTRACT words would not involve age-related feature binding mediated by the MTL. These predictions were confirmed by the results.
Our observations are consistent with the hypothesis that the structure of a category influences the consolidation of knowledge in semantic
memory.
 2003 Elsevier B.V. All rights reserved.
Theme: Neural basis of behavior
Topic: Neural plasticity
Keywords: Semantic memory; Memory consolidation; Concepts; Categories; Category specific effects; Feature binding; Medial temporal lobe;
Hippocampus; Neuroimaging
1. Introduction
The temporally-graded nature of retrograde amnesia
implicates the hippocampal formation in the initial acquisition of knowledge [73,82]. As this knowledge accrues in
memory, it becomes consolidated over time, thereby
establishing an enduring neocortical representation [48,57].
While various models of consolidation have debated the
details of this process [64,65], there is considerable
evidence that knowledge becomes consolidated in the
cerebral cortex through a process mediated by perihippocampal structures in the medial temporal lobe (MTL)
such as the subiculum, dentate gyrus, parahippocampal
*Corresponding author. Tel.: 11-215-895-1895; fax: 11-215-7628625.
E-mail address: [email protected] (J. Kounios).
0926-6410 / 03 / $ – see front matter  2003 Elsevier B.V. All rights reserved.
doi:10.1016 / S0926-6410(03)00164-2
cortex, perirhinal cortex, and entorhinal cortex [23]. Recent functional neuroimaging studies provide additional
support for the claim that MTL structures participate in the
formation of long-term memories [37,54,76].
Most of the debate about the mechanisms of consolidation has been concerned with episodic memory (i.e.
memory for past experiences). In contrast, the possible
consolidation of semantic memory (i.e. memory for word
meanings, concepts, and knowledge about the world) has
received less attention. The primary source of evidence for
semantic memory consolidation is found in the patient
literature. For instance, MTL lesions can result in temporally-graded retrograde amnesia for (nonautobiographical) facts, depending on the extent of the lesions [71]. This
retrograde amnesia presumably results from the interruption of an ongoing consolidation process mediated by the
MTL. Furthermore, hippocampal damage can impair rapid
acquisition of semantic information more than it impairs
J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
slow learning of semantic information over multiple
presentations, suggesting that the hippocampus is particularly important to the initial acquisition of information,
though eventual neocortical consolidation can apparently
proceed even without hippocampal participation, albeit in a
degraded fashion [42]. Additional evidence comes from
Semantic Dementia patients, where imaging studies and
pathologic analyses implicate damaged or dysfunctional
MTL structures [16,38,63]. Patients with Semantic Dementia exhibit a semantic memory deficit in which they
show more difficulty naming objects whose labels have a
later age of acquisition [52]. Although other work emphasizes the contribution of autobiographical memory to
apparent graded effects in semantic memory [81,89], these
observations are nevertheless consistent with the notion
that semantic knowledge acquired at an earlier age has had
more time to be consolidated in memory before disease
interrupted the consolidation process.
Studies of the neuroanatomy of semantic memory have
yielded evidence that different categories of knowledge are
consolidated in different brain areas. Although there is
some inconsistency across studies [13], patients with
disease affecting left ventral temporal-occipital cortex
often appear to be relatively compromised in their comprehension of natural kinds such as ANIMALS (where
capital letters refer to a concept) [20,26,27,39,68,84],
while disease compromising left lateral temporal-occipital
and left inferior and lateral frontal cortices often appears to
diminish comprehension of manufactured artifacts such as
IMPLEMENTS [11,20,21,33,40,61,78,80,87]. Support for
this category-specific distinction has also come from
functional neuroimaging work with healthy adults. Although debate persists concerning the reliability and
interpretation of such activation patterns [46], these studies
generally demonstrate recruitment of ventral temporaloccipital cortex for natural kinds [12,17,20,56,67] and
activation of left lateral temporal-occipital [12,20,56,59]
and left inferior-lateral frontal regions [32,34,56,67] for
manufactured artifacts.
The mechanisms by which semantic information apparently becomes distributed in these particular brain regions
remain a matter of active investigation. Based on known
primary connections in the areas yielding activation, the
‘sensory-motor’ hypothesis attributes category-specific differences to the presumed perceptual and motor-related
features contributing preferentially to each category of
knowledge [2,56]. For example, knowledge of visual–
perceptual features is hypothesized to be an important
characteristic of natural kinds such as ANIMALS, because
this visual–perceptual information is important for distinguishing between different types of ANIMALS; knowledge of ANIMALS is consequently associated with the
visual–perceptual processing stream in ventral temporaloccipital cortex. Likewise, visual–motion and motor–action features are said to be important attributes of manufactured artifacts; knowledge of IMPLEMENTS is thus
485
related to lateral temporal-occipital [6,50,66,70] and inferior-lateral frontal regions [45,74,75] associated with
visual–motion and motor–action, respectively.
Recent investigations have cast some doubt on the
sensory-motor account as a complete explanation of category-specific effects [13,58,85]. For example, patients with
a deficit for natural kinds do not necessarily have a
disproportionate impairment for processing information
about visual–perceptual features compared to motor-action
features [51,53,62,79]. Functional neuroimaging studies
also raise questions about the sensory-motor account. For
example, healthy young adults show activation in left
posterolateral temporal cortex and left prefrontal cortex for
both IMPLEMENTS and for ABSTRACT nouns having
few sensory-motor features [5,35]. Other studies relate
activation in left prefrontal cortex to the difficulty or
complexity of semantic access rather than to the representation of motor features [30,35,86]. Such results suggest
that the sensory–motor theory of concept representation is,
at best, incomplete, and that other principles are likely
involved.
An alternate account of category-specific effects turns
on the observation of important structural differences
among categories of knowledge. It appears that naturalkinds categories such as ANIMALS consist of shared and
overlapping features that are more highly intercorrelated
than is the case for manufactured artifacts such as IMPLEMENTS [22,31,58,85]. For instance, if an ANIMAL has
feathers, then it probably has a beak also; however, if an
IMPLEMENT has a handle, this does not necessarily
imply that it has a button as well. Such structural differences among categories may also contribute to the patterns
of brain activation associated with specific categories of
knowledge. In particular, the overlapping, intercorrelated
visual features of ANIMALS may enable the neural
representation of ANIMAL knowledge relatively early in
the visual processing stream [35]. This hypothetical mechanism may be related to genetically determined adaptive
pressures such as the recognition of potential predators or
food [14].
In the following study, we test the hypothesis that
differences among categories of knowledge are reflected,
in part, by the mechanisms through which knowledge of
these categories becomes consolidated in the brain. Toward this end, we measured patterns of brain activation in
healthy seniors in response to ANIMAL, IMPLEMENT,
and ABSTRACT words and compared these activation
patterns with those obtained from young adults, with
special attention to the MTL. Our rationale in comparing
category-specific patterns of brain activation from healthy
seniors to that of young adults is that consolidation, which
can take place over decades [37,73], should increase with
time. This increasing consolidation should result in less
MTL involvement with age. However, based on considerations discussed above, there are reasons to believe that the
consolidation process and the associated MTL recruitment
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J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
should also depend on the particular category of knowledge.
First, words of different semantic categories typically
vary in age of acquisition, a factor known to influence
semantic information processing [10]. For instance, concrete words such as ANIMALS and IMPLEMENTS are
acquired relatively early, while ABSTRACT nouns appear
to be acquired later [28,55]. All things being equal, such
concrete words should therefore consolidate at an earlier
age. However, we hypothesize that a second likely influence on semantic memory consolidation may result from
structural differences between the ANIMAL and IMPLEMENT categories, and that this factor is probably as potent
an influence on consolidation as age of acquisition. Such
concrete categories have usually been described as collections of linked features [72]. As mentioned above, previous
work has shown the ANIMAL category to consist of
overlapping and intercorrelated features to a greater extent
than the IMPLEMENT category, implying that the links
between ANIMAL features in semantic memory are
generally stronger than the links between IMPLEMENT
features [58,85]. One prominent view of the role of the
hippocampal formation is that this structure provides
temporary links between features represented in various
neocortical areas, and that consolidation occurs as these
initially diffuse neocortical feature representations are
‘weaned’ off of MTL-mediated feature binding as direct
links develop among their constituent features [4,64]. This
view could be extended to predict that categories naturally
consisting of highly intercorrelated (i.e. neocortically
interlinked) features should consolidate more quickly and
easily than categories consisting of relatively uncorrelated
features, because less MTL mediation of feature links
should be necessary for high-intercorrelation categories.
From this perspective, ANIMALS should generally be
consolidated relatively early and easily and therefore
exhibit little or no MTL activation in either young adults
or seniors. By comparison, the acquisition and neural
representation of IMPLEMENTS may involve relatively
greater MTL activation in children or young adults than in
healthy seniors. This is because it should take additional
time for knowledge of IMPLEMENTS to become fully
consolidated in young adults, while an additional halfcentury of consolidation is likely to reduce or virtually
eliminate MTL activation for this category in seniors.
Consequently, there should be differential age-related
MTL activation only for IMPLEMENTS.
To summarize, we predicted that ANIMALS and IMPLEMENTS would elicit little or no significant MTL
activation in older subjects, because both of these
categories of knowledge should be consolidated in these
subjects. In contrast, younger subjects should show evidence of MTL activation relative to older subjects specifically for IMPLEMENTS because this category has a
structure that may make consolidation slower or harder.
ABSTRACT nouns were also included in this experi-
ment for exploratory reasons. Little is known about the
neural substrates of abstract nouns that could suggest a
specific prediction about their consolidation over time
[5,35,41,47,49]. Abstract categories are, however, thought
to be qualitatively different from concrete ones in that each
abstract category consists of a system of semantic relations
into which different sets of features may fit, rather than
consisting of a single, relatively fixed set of linked
sensory-motor features [72]. Knowledge associated with
ABSTRACT nouns appears to be modulated by fluid
networks of propositions that are highly context dependent
[29,44,69]. According to this view, ABSTRACT nouns
may exhibit less binding-or consolidation-related MTL
activity at any age because of the dynamic, contextdependent nature of these words and their minimal sensory-motor content.
2. Materials and methods
2.1. Participants
Participants included sixteen healthy right-handed
seniors (seven females and nine males) with a mean age of
73.9 years and a mean education of 13.8 years. These
seniors received a thorough medical screening to rule out
conditions that could affect cognitive functioning. The
comparison group of young adults consisted of sixteen
right-handed native English speakers who were students at
the University of Pennsylvania (analyses of data from the
comparison group have been discussed elsewhere [35]).
This sample, tested at the same time as the seniors,
consisted of nine females and seven males, with a mean
age of 23.4 years and a mean education of 16.0 years.
None of the subjects were taking any sedating or centrallyacting medication at the time of testing. Structural images
obtained at the time of the fMRI study for the purpose of
normalization were reviewed to rule out structural brain
insult. Subjects participated in an informed consent procedure approved by the IRB of the University of Pennsylvania.
2.2. Stimulus materials
We presented blocks of printed words to subjects that
included ANIMAL, IMPLEMENT, and ABSTRACT
nouns. There were 60 words of each noun type, matched
for mean frequency [IMPLEMENTS513.1, ANIMALS5
12.3, ABSTRACT514.7, F(2,177)50.18, ns] and mean
letter length [IMPLEMENTS56.1, ANIMALS55.9,
ABSTRACT56.3, F(2,177)50.44, ns] [25]. A cohort of
42 native English speaking undergraduates assessed the
words for familiarity. All word meanings were known to
all students. All but seven (3.8%) of the words were
judged to be familiar by over 93% of these students.
Specifically, one animal was judged familiar by only 86%
J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
of the undergraduates, three abstract nouns were judged
familiar by only 88%, two abstract nouns were judged
familiar by only 79%, and one abstract noun was judged
familiar by only 76% of the students. The words were
either unambiguously nouns, or if not, a word’s frequency
of occurrence as a noun was at least five times that of its
verb homonym, according to form class-sensitive frequency measures [25]. To obtain age of acquisition data
for our stimuli, we probed twenty young adults [eight
males, twelve females; mean (6S.D.) age521.1 (64.9)
years; mean (6S.D.) education514.1 (63.3) years] using
a judgment technique validated by actual age of acquisition
observations of children [60]. Mean (6S.D.) age of
acquisition for the words in these categories is:
ANIMALS557.62 (620.3) months; IMPLEMENTS5
67.71 (621.8) months; and ABSTRACT5115.32 (620.6)
months (all pairwise comparisons differing significantly at
the P,0.01 level, according to t tests).
2.3. Procedure
To minimize the potential confounds of covarying
categories of knowledge and processes that access this
knowledge, we employed a relatively neutral task that
encouraged uniform processing across categories. Subjects
were thus asked to make ‘pleasantness’ decisions for each
item [35]. This task has been used for over 30 years to
probe or activate ‘deep’ or ‘semantic’ knowledge associated with words while avoiding a request for specific
information [43,88].
Each stimulus word was displayed for 3 s followed by a
1-s interstimulus interval. Words were presented sequentially, blocked by type, with each 10-word block lasting 40
s. Blocks were presented in a fixed random order with no
overt indication of where blocks began or ended. Pleasantness judgments were also made on two baseline blocks of
pronounceable pseudoword stimuli and four blocks of filler
words (verbs) which were interspersed among the noun
blocks (and which were equated to the nouns for word
length and, in the case of the verbs, for frequency).
(Results from the verb blocks will be discussed in a
separate report.) Subjects were not informed that different
categories of words were being administered. Three runs
containing nonrepeated stimuli were presented, each run
including two blocks of each word category. Subjects
indicated their judgment for each word by right- or lefthand button press for, respectively, ‘pleasant’ or ‘not
pleasant’ decisions. Response type and latency were
recorded by the computer presenting the stimuli. Before
each run, subjects were acclimated to the MRI environment by viewing the words ‘Get Ready’ on screen for 20 s.
Brief rest periods were included between runs.
Our stimulus presentation system, compatible with high
magnetic fields, backprojected the printed words onto a
screen at the magnet bore. The subject viewed the screen
through a system of mirrors. A portable computer (Macin-
487
tosh 1400C or G3) outside the magnet room used PSYSCOPE
presentation software [18] to present stimuli and record
response accuracies and latencies. Subjects were familiarized with the task prior to entering the magnet bore, and
the task was practiced by each subject.
2.4. Image acquisition and statistical analysis
Imaging was executed at 1.5 T on a GE Echospeed
scanner capable of ultrafast imaging. We used a standard
clinical quadrature radiofrequency head coil. Firm foam
padding was used to restrict head motion. Each imaging
protocol began with a 10–15 min acquisition of 5-mm
thick adjacent slices for determining regional anatomy,
including sagittal localizer images (TR5500 ms, TE510
ms, 1923256 matrix), T2-weighted axial images (FSE,
TR52000 ms, TEeff585 ms), and T1-weighted axial
images of slices used for fMRI anatomic localization
(TR5600 ms, TE514 ms, 1923256 matrix). Gradient
echo echoplanar images were acquired for detection of
alterations of blood oxygenation accompanying increased
mental activity. All images were acquired with fat saturation, a rectangular FOV of 20315 cm, flip angle of 908, 5
mm slice thickness, an effective TE of 50 ms, and a
64340 matrix, resulting in a voxel size of 3.7533.7535
mm. The echoplanar acquisitions consisted of 18 contiguous slices covering the entire brain every 2 s. To manage
susceptibility artifact, a separate acquisition lasting 1–2
min was needed for phase maps to correct for distortion in
echoplanar images [3]. We also inspected the raw data of
individual subjects. Raw data were stored by the MRI
computer on DAT tape and then processed off-line.
Initial data processing was carried out with Interactive
Data Language (Research Systems) on a Sun Ultra 60
workstation. Raw image data were reconstructed using a
2D FFT with a distortion correction to reduce artifact due
to magnetic field inhomogeneities. Individual subject data
were then prepared for pseudosubject analysis and analyzed statistically using statistical parametric mapping
(SPM 99) developed by the Wellcome Department of
Cognitive Neurology [24]. This system, operating on a
MATLAB platform, combines raw difference images from
individual subjects into a statistical t-score map. Briefly,
the images in each subject’s time series were registered to
the initial image in the series. The images were then
aligned to a standard coordinate system [83] using the
Montreal Neurological Institute template. The data were
spatially smoothed with a 12-mm Gaussian kernel to
account for interindividual differences in gyral anatomy
and small variations in the location of activation across
subjects, and low-pass filtering was implemented by
controlling autocorrelation with a first-order autoregressive
method. Global means were normalized by proportional
scaling. The data were analyzed parametrically using t-test
comparisons converted to z scores for each compared
voxel. We report differences between conditions that are
J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
488
Table 1
Proportion of ‘pleasant’ responses and response latencies (in milliseconds) from young adults and healthy seniors for implement, animal,
and abstract nouns
Category
Implements
Animals
Abstract
Young adults
more quickly by seniors than by young adults [t(29)52.03;
P,0.05].
Young adults judged IMPLEMENTS to be less pleasant
than ANIMALS [t(15)52.90; P,0.01]. By comparison,
healthy seniors judged IMPLEMENTS to be more pleasant
than ANIMALS [t(14)53.73; P,0.005] and ABSTRACT
nouns [t(14)52.28; P,0.05]. IMPLEMENTS [t(29)5
4.46; P,0.001] and ABSTRACT nouns [t(29)53.00; P,
0.01] were judged more pleasant by seniors than young
adults. These observations may suggest age-related effects
on pleasantness judgments.
Healthy seniors
Judgment
Latency
Judgment
Latency
0.60 (0.21)
0.71 (0.17)
0.69 (0.14)
1324 (239)
1210 (211)
1303 (205)
0.90 (0.15)
0.80 (0.17)
0.83 (0.12)
1159 (211)
1235 (206)
1282 (175)
Data are expressed as mean (6S.D.); due to equipment malfunction, the
behavioral data for one of the senior participants was lost. Consequently,
the means represent 16 young adults and 15 healthy seniors.
3.2. Imaging data
statistically significant at least at the P,0.05 level following correction for multiple comparisons for both the height
and the extent of activation, unless otherwise stated.
Table 2 summarizes the anatomical locations and extent
of the peak activations of each cluster that exceeded our
statistical threshold for pleasantness judgments for each
category of knowledge in healthy seniors. Images illustrating activation patterns for each category of knowledge in
comparison to a pronounceable pseudoword baseline are
provided in Fig. 1. As can be seen, significant activations
associated with the category of IMPLEMENTS are found
in left posterolateral temporal-parietal cortex, left inferior
frontal cortex, and the caudate. This pattern of categoryspecific activation was evident regardless of the baseline
condition (pronounceable pseudowords, or other word
categories). This replicates the anatomic distribution of
activation for IMPLEMENTS using the identical stimuli in
young adults [35]. By comparison, activations associated
with the ANIMALS-minus-pseudowords contrast recruited
left ventral temporal-occipital cortex in the area of the
lingual and fusiform gyri. This again replicates the
3. Results
3.1. Behavioral data
Mean pleasantness ratings and mean response latencies
associated with each category of words are shown in Table
1. The results yielded no evidence of age-related slowing.
Young adults judged ANIMALS more quickly than IMPLEMENTS [t(15)53.35; P,0.005], and ABSTRACT
nouns [t(15)52.76; P,0.05]. Healthy seniors judged
IMPLEMENTS more quickly than ANIMALS [t(14)5
2.48; P,0.05] and ABSTRACT nouns [t(14)52.85; P,
0.01]. Of particular note, IMPLEMENTS were judged
Table 2
Locus and extent of peak activations during pleasantness judgments of word categories in healthy seniors
Contrast
Activation locus (Brodmann area)
Coordinates
x
y
Activation extent
([ voxels)
Z
value
Corrected
P value
z
IMPLEMENTS2
PSEUDOWORDS
Left posterolateral temporal-parietal (40, 39, 22)
Left inferior frontal (44, 6)
Right caudate
244
232
8
244
12
212
48
8
20
1891 a
1891 a
1891 a
6.06
4.65
4.46
0.001
0.006
0.02
IMPLEMENTS2
ANIMALS
Left posterolateral temporal (39, 22)
Left inferior frontal (44, 6)
Right caudate
256
232
8
240
12
216
20
12
28
535
1364 a
1364 a
4.79
4.76
5.06
0.003
0.004
0.001
IMPLEMENTS2
ABSTRACT
Left posterolateral temporal (22)
Left inferior frontal (44, 6)
Right caudate
252
232
8
228
12
220
16
12
24
1695 a
1695 a
1695 a
4.07
5.05
4.58
0.055
0.001
0.008
ANIMALS2
Left ventral temporal-occipital (19)
PSEUDOWORDS
216
264
24
105
4.73
0.004
ANIMALS2
IMPLEMENTS
Left ventral temporal-occipital (19)
212
256
28
138
4.16
0.04
ANIMALS2
ABSTRACT
Right inferior frontal (47)
32
40
28
273
4.90
0.002
ABSTRACT2
IMPLEMENTS
Right inferior frontal (45, 44)
48
20
12
100
4.23
0.03
a
For the specified contrast, these peaks are part of the same large cluster.
J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
489
Fig. 1. Activations for noun categories in comparison to a pronounceable pseudoword baseline in healthy seniors. (A) IMPLEMENTS; (B) ANIMALS.
anatomic distribution of activation seen in young adults for
this category of knowledge using the identical stimuli [35].
For the ABSTRACT-minus-pseudowords contrast in healthy seniors, we observed activation that did not meet our
statistical threshold in left lateral temporal-parietal cortex
(x5248, y5236, z544; z score53.29, P,0.001, uncorrected) and in left occipital cortex (x528, y5268,
z516; z score53.54, P,0.001, uncorrected). Nevertheless, this also replicates the anatomic distribution of
activation seen with the identical stimuli in young adults
[35]. Right inferior frontal activation was seen for ANIMALS and ABSTRACT nouns when other word
categories were used as a baseline.
Table 3 and Fig. 2 summarize direct comparisons of
these normalized contrasts with the corresponding normalized contrasts in young adults. For the IMPLEMENTSminus-pseudowords contrast, young adults recruited the
MTL region significantly more than healthy seniors.
Greater activation that was marginally significant was
observed in left MTL in young adults compared to healthy
seniors for both the IMPLEMENTS-minus-ABSTRACT
contrast [x5224, y50, z5212; z score53.91, P,0.0001,
uncorrected] and the IMPLEMENTS-minus-ANIMALS
contrast [x5224, y50, z5212; z score53.49, P,0.001,
uncorrected]. Healthy seniors, by comparison, activated the
left cingulate and caudate significantly more than young
adults for the IMPLEMENTS-minus-pseudowords contrast
and the IMPLEMENTS-minus-ANIMALS contrast. There
were no age-related differences for the contrasts involving
ANIMALS and ABSTRACT nouns.
4. Discussion
The present study investigated the possibility of consolidation in semantic memory paralleling current conceptions
of episodic memory consolidation. Our strategy was to
assess MTL activation in healthy older adults relative to
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J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
Table 3
Locus and extent of peak activations in brain regions during pleasantness judgments of word categories comparing healthy seniors and young adults
Contrast
Activation locus (Brodmann area)
Coordinates
x
Young adults minus healthy seniors
IMPLEMENTS2
Left medial temporal-hippocampus (28)
pseudowords
IMPLEMENTS2
ABSTRACT
Left medial temporal-hippocampus (28)
Healthy seniors minus young adults
IMPLEMENTS2
Left cingulate-caudate (24, 23)
pseudowords
IMPLEMENTS2
ABSTRACT
Left cingulate-caudate (24, 23)
Activation extent
([ voxels)
y
Z value
Corrected
P value
z
224
24
28
94
4.20
0.03
224
0
212
54
3.91
0.07
220
212
32
344
4.08
0.04
220
28
28
385
5.00
0.001
young adults during retrieval of semantic information from
different categories, with the presence of MTL activation
being taken to indicate that the information being retrieved
is not fully consolidated in the neocortex. Greater MTL
activation was predicted for object categories in younger
subjects than for older ones, because more consolidation
has presumably taken place in older subjects. Moreover,
based on a straightforward extension of standard consolidation theory, this effect was predicted to be categoryspecific: We predicted greater MTL activation in young
adults specifically for IMPLEMENTS but not for ANIMALS or ABSTRACT nouns. This was hypothesized to
have occurred because consolidation of the category of
IMPLEMENTS does not benefit from the ANIMALS
category’s high feature intercorrelations or overlapping of
features across exemplars.
The main findings can be summarized as follows. First,
the present results from healthy seniors replicate previous
neuroimaging findings of category-specific effects from
young adults reviewed in the Introduction. Specifically,
significant activations associated with the category of
IMPLEMENTS in healthy seniors included left posterolateral temporal cortex and left inferior frontal cortex. By
comparison, the category of ANIMALS in healthy seniors
recruited left ventral temporal-occipital cortex.
Second, the major prediction of greater category-specific
MTL activation in young adults compared to healthy
seniors was borne out. Thus, young adults had significantly
greater MTL activation than healthy seniors for IMPLEMENTS but not for ANIMALS. This finding was not
dependent on a particular baseline, as it was evident
relative to both the pseudoword and ABSTRACT
baselines. Furthermore, these activation patterns may have
an analog in the behavioral results. Mean reaction time for
IMPLEMENTS was faster for seniors than for young
adults, while the mean reaction times for ANIMALS and
ABSTRACT words did not differ significantly for seniors
and young adults. This suggests that the apparently incomplete consolidation of IMPLEMENTS in young adults
resulted in a cost in speed of information processing
relative to the seniors. In sum, these findings are consistent
with the notions of differential consolidation of semantic
categories depending on category structure and evolutionary significance.
Several additional points should be noted about these
results. First, the view we have developed here implies that
the contrast of IMPLEMENTS minus ANIMALS should
reveal MTL activation in young adults. We may not have
observed this in our previous work [35] because ANIMALS may elicit some small, but statistically nonsignificant, MTL activation in young adults which obscured MTL
activation for IMPLEMENTS relative to ANIMALS.
Because the semantic consolidation theory tested here
predicts such an effect, additional work with larger numbers of young subjects is needed to examine this point
more rigorously.
Second, the present results cannot be attributed to
seniors generally exhibiting less brain activation during
such tasks. Not only does the category-specific nature of
the predicted effect argue against this interpretation, but
normalization removed global activation differences between the seniors and young adults. Furthermore, the fact
that seniors exhibited greater relative activation than
younger subjects in the caudate and left cingulate for the
IMPLEMENTS minus pseudowords and IMPLEMENTS
minus ABSTRACT contrasts weighs against any explanation based on general lack of activation for seniors. The
caudate plays a central role in several frontal–striatal–
thalamic loops that may be implicated in age-related
activation associated with IMPLEMENTS [1]. It is unclear
at present whether this finding reflects actual changes in
processing mechanisms or storage sites of specific types of
semantic information during healthy aging, or whether it
reflects compensatory activity in support of diminished
semantic information processing with age. For example,
recruitment of the caudate has been associated with both
the representation of motor knowledge [36] and with
age-related upregulation of working memory in support of
J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
491
Fig. 2. Direct contrast of young adults and healthy seniors for IMPLEMENTS. (A) IMPLEMENTS-minus-pseudowords in young adults minus healthy
seniors (z516); (B) IMPLEMENTS-minus-pseudowords in healthy seniors minus young adults.
language processing [19,77]. However, the fact that seniors
responded to IMPLEMENTS more quickly than young
adults weighs against the compensation explanation and in
favor of the notion that the processing mechanisms or
storage sites of IMPLEMENT information may change
with age. Activation of the cingulate has been associated
with executive resources such as selective attention and
control over resource deployment during decision-making
[7,8,15], and healthy seniors may depend more on activation of brain regions supporting these resources than young
adults, especially for IMPLEMENTS, because the relatively diffuse feature structure of this category may, even
with greater neocortical consolidation in seniors, require a
larger share of limited processing resources.
Third, the present results are unlikely to be due to an
inability by the healthy seniors to activate the MTL in
response to any semantic category. Assuming that the
MTL activation to IMPLEMENTS in the young adults
plays some functional role (i.e. the standard assumption of
neuroimaging and psychophysiological research), the fact
that the seniors, who yielded little MTL activation, exhibited no deficit in behavioral performance (in fact, they
responded more quickly to IMPLEMENTS than did the
young adults) suggests that their relative lack of MTL
activation was not due to age-related deterioration, but
rather to a quantitative change corresponding to consolidation. This notion is supported by the fact that the seniors’
overall patterns of brain activation in response to the three
492
J. Kounios et al. / Cognitive Brain Research 17 (2003) 484–494
categories of words were generally quite similar to those of
the young adults.
Fourth, though our results include null findings such as
the absence of significant MTL activation for the seniors,
neither the present study nor the semantic memory consolidation model tested here depend on the logic of null
hypothesis testing. The key finding that the young adults
exhibited greater MTL activation to IMPLEMENTS than
did the seniors is predicted by the semantic consolidation
model; the fact that the seniors yielded a nonsignificant
level of MTL activation does not negate this point. This
model derives further support from the finding of faster
reaction times to IMPLEMENTS in seniors than in young
adults. More generally, the lack of significant MTL
activation in the seniors, while a null finding, is not
problematic for future tests of the theory, as the theory
only predicts less MTL activation in seniors than in young
adults and does not necessarily predict the absence of MTL
activation (though such an absence would not be inconsistent with the theory). Nevertheless, further research testing
for graded MTL effects across several age groups would
provide a useful and more stringent test of the theory.
Fifth, as is the case for virtually all semantic memory
research, a caveat must be given concerning the stimuli
used in the present study. Although the words selected
from the ANIMALS and IMPLEMENTS categories were
carefully equated along several dimensions, there is always
the possibility that some unknown, uncontrolled stimulus
factor was driving the results rather than these findings
being caused by the different category structures revealed
by prior research. Future studies using different stimuli
will help to generalize these findings beyond the present
stimulus set, thereby reducing the likelihood that ancillary
factors were influencing the results.
And sixth, although we cannot yet assert that the present
results are generalizable beyond the pleasantness task we
adopted in this study to other tasks, we believe that future
efforts with other tasks will replicate our findings (for a
discussion of issues related to the pleasantness task, see
[35]). There is no a priori reason to believe that IMPLEMENTS are more likely to be associated with an affective
connotation than animals, and while we are not aware of
any evidence directly addressing the relative capacity of
IMPLEMENTS and ANIMALS to adopt an affective
connotation, our intuition is that ANIMALS are more
likely to be associated with an affective connotation than
IMPLEMENTS. Although we cannot rule out the possibility that increased MTL activation in young adults is
related to category-specific difficulty in labeling IMPLEMENTS with a pleasantness value, we are not aware of
any evidence consistent with this kind of effect.
Finally, ABSTRACT words did not exhibit significant
MTL activity, even though such words have a later age of
acquisition than ANIMAL or IMPLEMENT words. Cognitive psychology and neuroscience provide little foundation
on which to base relevant speculation about ABSTRACT
words beyond some theoretical and empirical evidence that
ABSTRACT categories are qualitatively different from
CONCRETE categories such as ANIMALS and IMPLEMENTS [9]. Assuming that the MTL mediates linkage of
concept features across various neocortical areas during
concept acquisition, the absence of detectable MTL activity associated with ABSTRACT words in either younger or
older subjects is consistent with the observation that
ABSTRACT categories differ from CONCRETE
categories in some fundamental way, such as a lack of
sensory–motor content and the flexible, context-dependent
nature of semantic representations associated with ABSTRACT nouns [29,44,69,72].
In conclusion, the present study demonstrates categoryspecific, age-related MTL activation in semantic memory
consistent with current notions of the role of the MTL in
feature binding and consolidation of episodic memory.
These results also suggest that knowledge structure is an
important influence on consolidation. Finally, these results
not only provide an important point of similarity between
semantic and episodic memory, thereby suggesting common mechanisms and structure, but they highlight the fact
that semantic memory is dynamic in nature, rather than
being a static repository of concepts and facts.
Acknowledgements
This work was supported in part by the US Public
Health Service grants AG15116 and AG17586 to M.G.,
and DC04818 and MH57501 to J.K.
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