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The Hub-and-Spoke Hypothesis of Semantic Memory

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S E C T I O N K

CONCEPTUAL SEMANTIC
KNOWLEDGE

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C H A P T E R

c0061 61
The Hub-and-Spoke Hypothesis of Semantic
Memory
Karalyn Patterson1,2 and Matthew A. Lambon Ralph3
1
Neurology Unit, Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK; 2MRC Cognition
and Brain Sciences Unit, Cambridge, UK; 3Neuroscience and Aphasia Research Unit, School of Psychological Sciences,
University of Manchester, Manchester, UK

s0010
61.1 INTRODUCTION
p0010 The quantity of, quality of, and speed of access to
semantic knowledge in the human brain is astonishing.
Given any fragment of information, such as the word
“camel,” a healthy adult human can almost instantly
generate a vast amount of other related information,
such as the ways in which camels are and are not like
other animals, how they look and move, where they
live, how they interact with people, that it is the name
of an American brand of cigarettes, that they are the
subject of a famous story by Rudyard Kipling (How the
Camel Got His Hump), and so forth. Curiously, this kind
of conceptual knowledge—although often discussed by
philosophers—did not become a major topic of research
in cognitive science and neuroscience until relatively
recently. Endel Tulving put it on the psychological map
in 1972, when he proposed that semantic memory was
a qualitatively different kind of knowledge from the
episodic memory typically studied by experimental
psychologists at that time. Elizabeth Warrington put
it on the neuropsychological map in 1975, when she
demonstrated that brain disease could selectively
impair semantic memory. Now, approximately 40 years
later, semantic memory is a commonplace object of
behavioral study, brain research, and theorizing.
p0015 Over the past 15 20 years, we and our colleagues
have been developing a story about the structure and
neural basis of semantic memory that we call the hub-
and-spoke hypothesis (Lambon Ralph, 2014; Lambon
Ralph & Patterson, 2008; Lambon Ralph, Sage, Jones, &
Mayberry, 2010; Patterson, Nestor, & Rogers, 2007;
Rogers et al., 2004). The basic plot of this story comes in
two parts (Figure 61.1). First, many different modality-
specific cortical regions represent the aspects of con-
ceptual knowledge that are modality-specific: the color
of a camel in color regions, its shape in visual-form
regions, the way it moves in regions that code visual
movement, its name in language-specific cortex, and
so on. Second, all of these regions send information
to and receive information from a hub component
of the semantic network, which codes semantic similar-
ity structure and represents concepts in a manner
that abstracts away from the specific features of
how they look or sound or move or what they are
called. The links between each modality-specific region
and the hub are called spokes. Because it is the hub
part of this story that is (somewhat) novel, other
semantic-memory researchers—especially those critical
of this hypothesis—occasionally describe our theory
as one in which concepts have a completely abstract
form of representation and reside in the hub. For exam-
ple, Gainotti (2014) included our work in a short list of
models “that assume that semantic representations. . .
are stored in an abstract and propositional format”
(Gainotti, 2014, p. 7). We acknowledge that some earlier
expositions of our incompletely formed view may have
sounded a bit like this (Patterson & Hodges, 2000),
but it is certainly not an accurate description of our cur-
rent hub-and-spoke hypothesis about semantic memory.
We therefore begin the account of our position with
an explanation of the crucial spoke components of
the theory, called “the importance of the spokes and
the regions from which they emanate.” Sections 61.2
and 61.3 argue that, although essential, the spokes
and their modality-specific sources are insufficient and

Neurobiology of Language. DOI: http://dx.doi.org/10.1016/B978-0-12-407794-2.00061-4 3 © 2015 Elsevier Inc. All rights reserved.

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4 61. THE HUB-AND-SPOKE HYPOTHESIS OF SEMANTIC MEMORY

Olfaction Praxis

ATL modality-invariant
Sounds Somatosensory

Verbal descriptors Visual features

f0010 FIGURE 61.1 The “hub-and-spoke” model of conceptualization. Under this hypothesis, concepts are formed by the mutual interaction of
modality-specific sources of information (the “spokes”) with a central representational hub (red) that provides additional modality-invariant
representational resource. The spokes are assumed to rely on modality-specific secondary association cortical regions while regions within the
anterior temporal region (and, perhaps, other tertiary association areas) underpin the transmodal hub. Conceptualization follows from the
joint action of the hub and spokes (see text for further details). Various computational implementations of this framework have been described
in detail and demonstrate how concepts can be coded in this framework and how data from SD and patients with unilateral temporal lobe
damage can be mimicked. From Rogers et al., 2004 and Schapiro et al., 2013.

that a transmodal hub is also necessary. Section 61.4
addresses reasons for locating the proposed hub in
the anterior temporal lobe (ATL). Section 61.5 offers
evidence for the bilateral nature of the ATL hub.
Section 61.6, on the graded hub hypothesis, provides
some more specific suggestions about different roles for
various areas of the ATL.
s0015 61.2 THE IMPORTANCE OF THE
SPOKES AND THE REGIONS FROM
WHICH THEY EMANATE
p0020 It now seems almost incontrovertible that our
knowledge about the modality-specific sensory and
motor features of objects and other concepts is repre-
sented in or very near the same brain regions that pro-
cess such information when it is encountered in the
real world (Barsalou, 2008). This view, usually called
either grounded or embodied cognition, is endorsed in
one form or another by so many researchers that if we
were to try to mention all of them, the rest of this sec-
tion might consist of nothing but a list of references.
Several different forms of evidence converge to
support this idea, principally: (i) regionally specific
patterns of brain activation, observed in healthy parti-
cipants, that differ as a function of the modality or cat-
egory of the stimulus and/or response; (ii) patterns of
cognitive impairment, resulting from brain lesions in
different locations, that also differ in principled ways
depending on the sensory or motor features of the
stimulus or response; and (iii) data from transient dis-
ruption of neural function in different regions via tran-
scranial magnetic stimulation in neurologically intact
participants (Pobric, Jefferies, & Lambon Ralph,
2010b). To be sure, some specific claims about modal-
ity or category-specific effects are open to debate
(see Chen & Rogers, 2014, for a good discussion). To
be even more sure, brain function is almost infinitely
more subtle and complex than our limited ability to
study it and think about it (Patterson & Plaut, 2009).
This means that any claim for a simple relationship
between a specific category and a specific brain
region (e.g., “the fusiform face area [FFA] in the
right posterior temporal lobe is completely and
uniquely dedicated to processing faces”) is unlikely to
characterize the true state of things in the brain. We
already know that areas other than the FFA respond to
faces (Pitcher, Walsh, Yovel, & Duchaine, 2007) and
that damage to the FFA resulting in prosopagnosia
typically disrupts some abilities beyond face proces-
sing (Behrmann & Plaut, 2012). Nevertheless, there is a
considerable degree of sensory-feature and motor-
feature specialization in both processing and represen-
tation of different kinds of things that no theory of
semantic representation can ignore. And it is crucial to
emphasize that, according to embodied/grounded the-
ories, this specialization does not just reflect surface

K. CONCEPTUAL SEMANTIC KNOWLEDGE

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61.3 THE INSUFFICIENCY OF THE SPOKES AND THEIR SOURCES: WHY WE NEED A HUB
features of stimuli: words referring to concepts of dif-
ferent types can also produce both brain activations in
modality-relevant sensory or motor regions (Hauk,
Shtyrov, & Pulvermüller, 2008; Pulvermuller, 2005;
Simmons et al., 2007) (see de Zubicaray, Arciuli, &
McMahon, 2013 for an alternative interpretation of
some results that might seem to support necessary
activation in motor cortex when participants process
action words) and distinctive patterns of impairment
in patients with lesions in or near such sensory/motor
areas (Boulenger et al., 2008; Pulvermüller et al., 2010).
That is, a degree of specialization seems to apply to
the concepts or mental representations of objects, not
just objects in the real world.
p0025 In a useful review of “embodiment and the neuro-
science of semantics,” Meteyard, Cuadrado, Bahrami,
and Vigliocco (2012) placed various theories about
conceptual knowledge on an embodiment continuum,
from “strong” to “weak” to “secondary” to “absent.”
The previous paragraph summarizes our reasons for
rejecting theories that argue for purely abstract seman-
tic representations with no element of embodiment.
However, we also reject the most strongly embodied
theories for reasons described in the next section.
To summarize this first section, the hub-and-spoke
hypothesis suggests that semantic knowledge is repre-
sented in a widely distributed brain network including
modality-specific regions of cortex from which connec-
tions (spokes) emanate, sending activation to and receiv-
ing activation back from another essential component of
the network: a transmodal semantic hub.
s0020 61.3 THE INSUFFICIENCY OF THE
SPOKES AND THEIR SOURCES:
WHY WE NEED A HUB
p0030 Strongly embodied theories of conceptual knowl-
edge “effectively push semantics out into primary
cortical areas and make it completely dependent on
sensory and motor systems” (Meteyard et al., 2012,
p. 793). In other words, according to such theories,
the brain network for your knowledge of a concept
such as camel consists only of the specific sensory/
motor/linguistic features that you have experienced
concerning camels. How do strongly embodied theo-
ries account for the fact that, on hearing the word
“camel,” you can almost instantly generate all that
other information mentioned in the introduction? They
assume that all of the feature representations in the
modality-specific regions of cortex are connected to
one another. Hearing the word “camel” initially pro-
duces selective activation of an auditory/linguistic
representation; then, in a pattern-completion fashion,
K. CONCEPTUAL SEMANTIC KNOWLEDGE
Hickok-1611153 978-0-12-407794-2
5
activation rapidly spreads via the inter-area connec-
tions to other modality-specific aspects of your camel
knowledge. Straightforward enough, so why reject this
hypothesis?
First, consider semantic dementia (SD), a neurode- p0035
generative condition in the spectrum of frontotemporal
dementia. The characteristics of SD especially germane
to the current discussion—one neuroanatomical and
four behavioral/cognitive—are as follows:
1. All clinical diagnoses of neurological origin are o0010
associated with a degree, larger or smaller, of
variability across individual patients in “the three
S’s”: site, size, and/or side of lesion. This fact, of
course, makes it somewhat tricky to be confident
about the precise neuroanatomical basis of the
deficits. Such variability inevitably applies to SD,
but it is widely agreed among researchers of
neurodegenerative diseases that SD falls at the
lower end of this spectrum of variability, especially
in its early-middle phases (Acosta-Cabronero et al.,
2011; Guo et al., 2013; Mion et al., 2010). To quote
from Hodges and Patterson (2007), “Patients with
even early-stage SD show bilateral, though typically
asymmetrical, atrophy of the ATLs; as the disease
progresses, the degeneration extends either caudally
into the posterior temporal lobes or rostrally into
the posterior, inferior frontal lobes, or both.
Quantitative MRI studies. . .have refined these
observations by showing consistent and extreme
atrophy (commonly 50 80% gray matter loss) of
the polar and perirhinal cortices and the anterior
fusiform gyri (Davies, Graham, Xuereb, Williams, &
Hodges, 2004; Du, Schuff, & Kramer, 2007; Gorno-
Tempini, Dronkers, & Rankin, 2004)” (p. 1009). It
should be noted that the hippocampus and
entorhinal cortex are also substantially abnormal in
SD (Chan, Fox, & Rossor, 2002; Williams, Nestor, &
Hodges, 2005). Unlike the case of Alzheimer’s
disease (AD), however, the medial temporal
atrophy in SD is much more severe in the rostral
than in the caudal region. Why SD patients, despite
their hippocampal abnormality, do not have the
profoundly impaired anterograde amnesia
characteristic of AD is a fascinating and evolving
story (Nestor, Fryer, & Hodges, 2006; Nestor, Fryer,
Ikeda, & Hodges, 2003), but this is not especially
germane to this chapter on semantic memory.
Results of the multimodal imaging study of SD
patients and healthy controls by Guo et al. (2013),
in agreement with many other investigations of SD,
established that focal atrophy was confined to the
ATL bilaterally. The critical finding of Guo et al.,
however, is that this focal structural damage was
accompanied by reduced physiological integrity
00061
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6 61. THE HUB-AND-SPOKE HYPOTHESIS OF SEMANTIC MEMORY
in many or all of the modality-specific regions
demonstrated to be connected to the ATL in the
control participants. Furthermore, the patients’
semantic deficits correlated with both the ATL
atrophy and the reduced connectivity to more
specific regions. This one highly salient piece of
research thus supports the existence and necessity
of both the hub and the spokes. Guo et al. concluded
that their evidence favors a model of the semantic
network in which “a critical transmodal ATL
semantic hub [is] positioned to integrate functionally
relevant and topographically organized links to
distributed modality-specific regions” (p. 2,988).
o0015 2. At least in the prefinal stages of the disease, the
cognitive consequences of SD are largely confined
to disruption of semantic knowledge per se
(Guo et al., 2013; Hodges, Patterson, Oxbury, &
Funnell, 1992; Snowden, Goulding, & Neary, 1989;
Warrington, 1975) and of abilities in which semantic
memory plays an important interactive role
(Patterson et al., 2006).
o0020 3. The deterioration of semantic memory in SD is
pan-category and transmodal: different kinds of
concepts (e.g., concrete/abstract; living/human-
made) are all impaired, and the semantic deficits
are apparent no matter what format of stimulus
(object, picture, spoken word, written word,
environmental sound, taste, touch, etc.) is used to
probe for conceptual knowledge and no matter
what modality of response (pointing, speaking,
writing, drawing, etc.) is used to measure
performance (Bozeat, Lambon Ralph, Patterson,
Garrard, & Hodges, 2000; Rogers et al., 2004).
o0025 4. The pattern of the cognitive deficits in SD invariably
reflects an interactive impact of the familiarity or
frequency of the stimulus concept (i.e., how often a
concept is experienced) and the typicality of the
stimulus in its domain (i.e., how similar each
exemplar is to the category average or “prototype”).
In many diverse tests and tasks that have
manipulated the frequency and typicality of the
stimuli, significantly impaired and poorest
performance by SD patients is always observed for
atypical and less familiar stimuli/concepts (Lambon
Ralph et al., 2011; Patterson et al., 2006; Rogers
et al., 2004; Woollams, Cooper-Pye, Hodges, &
Patterson, 2008).
o0030 5. The nature of the errors made by SD patients is
anything but random and, in virtually any task,
their errors can be described as resulting from
failures of appropriate generalization and
discrimination (see Lambon Ralph & Patterson,
2008, for an extended discussion of such errors in
both receptive and expressive experimental tasks,
as well as in everyday life, and in both verbal and
K. CONCEPTUAL SEMANTIC KNOWLEDGE
Hickok-1611153 978-0-12-407794-2
nonverbal contexts). In object naming, for example,
instances of a category that are of moderate
familiarity and typicality can no longer be
discriminated correctly, resulting in errors such
as naming a fox as “dog” or a zebra as “horse” or
calling them both “animal.” But less familiar and
atypical animals such as a seahorse or a snail even
fail to be generalized to the animal category: they
usually result in content-less naming responses
such as “a little thing” or “I don’t know” or “what
do you do with that?” (Patterson et al., 2007;
Woollams et al., 2008). The same is true for object
and word categorization: typical things are
overgeneralized and atypical things are
undergeneralized (Mayberry, Sage, & Lambon
Ralph, 2011; Snowden, Griffiths, & Neary, 1996).
The first neuroanatomical characteristic indicates p0070
that the brain dysfunction in SD is typically centered on
the ATL, with consequent disruption to the integrity of
connections between the ATL and modality-specific
primary and association cortices. The last four neuropsy-
chological characteristics indicate that the cognitive
abnormality is relatively restricted to semantic memory
(and its impact on other tasks) and follows a highly con-
sistent pattern. Given this set of well-established obser-
vations, it seems difficult to construct an account of SD
that is compatible with a semantic network consisting
only of modality-specific sensory, motor, and language
regions of the brain. To our knowledge, there are no
reports of significant structural degradation of modality-
specific regions in SD. Furthermore, if SD did involve
widespread degeneration of modality-specific regions,
then it should yield cognitive deficits well beyond
semantic memory, as seen in AD. For example, visuo-
spatial processing depends substantially on parietal lobe
regions; AD patients have parietal hypometabolism/
atrophy with disrupted visuospatial ability; SD patients
have neither (Pengas et al., 2010). Finally, if the transmo-
dal semantic disorder in SD did arise from widespread
abnormalities to modality-specific regions, then why
would the pattern of disorder (the interaction between
familiarity and typicality and the nature of the errors) be
so consistent across all modalities and tasks? It seems
much more plausible that the deficits in SD all emerge
from disruption to a part of the semantic network that
codes conceptual space independent of any modality-
specific features of concepts in which the structure is
defined by similarity of instances within domains and
strongly influenced by familiar and typical instances
(Rogers et al., 2004).
SD provides a clear, potentially definitive line of p0075
evidence against the strongest embodied theories of
conceptualization, but it should also be noted that
some researchers in related fields (such as philosophy,
00061
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61.4 WHY SHOULD THE HUB BE CENTERED ON THE ATL?
e.g., Wittgenstein 1957, and cognitive science, e.g.,
Rosch, 1975; Smith & Medin, 1981) have also argued
that models based on modality-specific features alone
might be inadequate for the formation of coherent
concepts and categories. A full exposition of the various
arguments is beyond the scope of this chapter (these
can be found in Lambon Ralph, 2014; Lambon Ralph,
Sage, et al., 2010; Patterson et al., 2007; Rogers &
McClelland, 2004), but the kernel of the issue is that
the relationship between the abundance of modality-
specific information and the plethora of concepts that
emerge from them is highly complex and nonlinear.
Our key working hypothesis, implemented computa-
tionally (Rogers et al., 2004; Schapiro, McClelland,
Welbourne, Rogers, & Lambon Ralph, 2013) and sup-
ported neuroanatomically (Binney, Parker, & Lambon
Ralph, 2012; Guo et al., 2013), is that concepts represent
the joint action of distributed modality-specific regions
(the “spokes”) with an intermediate transmodal repre-
sentational region (the “hub”). The hub provides the
key additional computational capacity to draw the
multiple and complex sources of information together,
thereby deriving coherent and generalizable concepts.
s0025 61.4 WHY SHOULD THE HUB
BE CENTERED ON THE ATL?
p0080 The principal argument here is, unsurprisingly, that
the SD patients whose behavior strongly suggests the
existence of a semantic hub have atrophy consistently
centered on the ATL. It is worth noting that the best
hypothesis about the location of a semantic hub in
the ATL has changed somewhat since the earliest
AU:1 proposals. Because damage (e.g., as measured by VBM
analyses on structural MR images in SD) appears to
be maximal at the temporal pole (Brodmann area 38),
that was the originally suggested hub region (Hodges
et al., 1992; Patterson & Hodges, 2000). These earlier
studies did not have sufficient power—because of
relatively low patient numbers—to support correlations
between lesion location and semantic performance.
With improved diagnostic recognition of and further
research on SD, however, that limitation has begun to
recede, and the best evidence points to a region in
the ATL posterior to the temporal pole, the anterior
portion of the fusiform gyrus, which is subjacent to
the head and body of the hippocampus (Brodmann
areas 20 and 36). That is, atrophy and hypometabolism
are severe across the entire anterior temporal region
including both the temporal pole and this slightly more
posterior and inferior region; however, the abnormality
in the anterior fusiform correlates best with semantic
scores (Libon et al., 2013; Mion et al., 2010).
K. CONCEPTUAL SEMANTIC KNOWLEDGE
Hickok-1611153 978-0-12-407794-2
7
Because no one is satisfied with scientific proposals/ p0085
conclusions based on a single form of evidence, it is
fortunate that there are populations other than SD
patients and techniques other than the ones already
mentioned that are compatible with a transmodal
component of the semantic network located in the
ATL. In this context, it is vital to note that standard
fMRI—the source of most evidence concerning locali-
zation of function in the healthy brain—has been a
rather inadequate source of evidence concerning the
ATL because of various methodological limitations,
including MRI field inhomogeneities, limited field-
of-view, and the nature of the baseline task against
which semantic task performance is compared (Devlin
et al., 2000; Visser, Jefferies, & Lambon Ralph, 2010).
Functional imaging studies using full field-of-view
PET have often reported ATL activations when healthy
participants perform semantic tasks (Sharp, Scott, &
Wise, 2004; Vandenberghe, Price, Wise, Josephs, &
Frackowiak, 1996). Furthermore, the relevance of the
ATL to semantic knowledge is supported by recent
results from: (i) distortion-corrected fMRI of this
region (Visser, Jefferies, Embleton, & Lambon Ralph,
2012; Visser & Lambon Ralph, 2011); (ii) multivoxel
pattern analyses of fMRI data (Peelen & Caramazza,
2012); (iii) the application of rTMS to the lateral part
of this region (Lambon Ralph, Pobric, & Jefferies,
2009; Pobric, Jefferies, & Lambon Ralph, 2010a;
Pobric et al., 2010b; Pobric, Jefferies, & Lambon Ralph,
2007); and (iv) source-based analyses of MEG signals
(Marinkovic et al., 2003).
Three kinds of evidence combine to suggest that the p0090
ATL might constitute a reasonable location for a trans-
modal semantic hub. Findings from nonhuman primate
physiology (Gloor, 1997) and human functional and
structural connectivity studies (Binney et al., 2012; Guo
et al., 2013) indicate that a number of primary sensory
and motor areas, along with their related association
cortices, connect to and merge information in the
ATL. In addition to the rather factual nature of much
conceptual information, semantic memory is often “fla-
vored” by aspects of emotion and reward. Brain regions
vital to these aspects of experience, including the amyg-
dala and other limbic structures as well as the orbito-
frontal cortex, are also close and well-connected to
the ATL. The temporal lobe regions apparently impor-
tant in semantic memory are immediately adjacent
to the anterior parts of the medial temporal lobe mem-
ory system critical for rapid learning of new episodic
information. Conceptual knowledge, although mostly,
and for good reasons, acquired gradually (McClelland,
McNaughton, & O’Reilly, 1995), is ultimately based on
information experienced in episodes.
As a final note on this topic, it is potentially inter- p0095
esting and important that the center of the ATL
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8 61. THE HUB-AND-SPOKE HYPOTHESIS OF SEMANTIC MEMORY
transmodal hub (anterior fusiform/ITG) aligns with
previously separate literature on neurophysiological
evidence from patients who have depth or grid electro-
des surgically implanted as part of investigation and
treatment for long-term epilepsy. Ventral ATL regions
are often considered to be visually specific, reflecting
the apex of a visual “ventral” stream of processing
(Albright, 2012); however, the same area also appar-
ently plays a role in language processing. In their sem-
inal studies, Lüders et al. (1986, 1991) demonstrated
that stimulation of this region gave rise to transient
language impairment (of reading and naming) and,
consequently, they coined the term “basal temporal
language area.” Direct measurement of local field
potentials confirmed its role in naming (Nobre,
Allison, & McCarthy, 1994). More recent studies have
demonstrated that these regions show sensitivity to
semantic categories, but not low-level variations in
visual characteristics (e.g., orientation and size).
Strikingly, these semantic effects emerge very rapidly
(B120 ms) after the onset of the stimulus (Chan et al.,
2011; Liu, Agam, Madsen, & Kreiman, 2009). Although
further direct comparisons with SD patients and func-
tional neuroimaging are required, these data from the
cognitive neurosurgery literature appear to support
the hypothesis that this region is the centerpoint of
a transmodal semantic hub.
s0030 61.5 EVIDENCE FOR AND POSSIBLE
REASONS FOR A BILATERAL ATL HUB
p0100 So far, our attention has been on the ATL as a
whole and in the singular. In the next two sections we
consider emerging evidence for subdivisions both
within the ATL in each hemisphere, from dorsal to
ventral (see Section 61.6) and (in this section) across
the two hemispheres. The ATL abnormality in SD
patients is always bilateral (although often very asym-
metrical, at least until late in the disease), suggesting
that both left and right regions may contribute to
conceptual knowledge. Other patient groups with clini-
cally notable impairment of semantic memory typically
have bilateral ATL damage [e.g., AD (Hodges &
Patterson, 1995) and herpes simplex virus encephalitis
(Lambon Ralph, Lowe, & Rogers, 2007; Noppeney
et al., 2007)]. Likewise, formal meta-analyses of the
functional neuroimaging literature indicate that both
ATLs are implicated in semantic function in neurologi-
cally intact participants (Binder, Desai, Graves, &
Conant, 2009; Visser et al., 2010). These neuropsycho-
logical and neuroimaging results prompt the some
obvious but important questions. First, does semantic
impairment require bilateral ATL damage? And, if so,
then what are the roles of the left versus right ATL?
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Hickok-1611153 978-0-12-407794-2
Recent studies that have explored semantic function p0105
in patients with unilateral ATL damage indicate that
semantic performance is generally much better than in
patients with bilateral ATL diseases, especially SD.
With more sensitive assessments, however, expressive
and receptive semantic deficits can be observed after
unilateral ATL lesions (Bi et al., 2011; Lambon Ralph,
Cipolotti, Manes, & Patterson, 2010; Lambon Ralph,
Ehsan, Baker, & Rogers, 2012). These contemporary
studies fit with the older comparative neurology litera-
ture that consistently reported chronic multimodal
(visual and auditory) “semantic” impairment in
primates and monkeys after bilateral ATL resection,
but only a milder and transient form of the same
impairment after unilateral resection (Brown &
Schafer, 1888; Klüver & Bucy, 1939). Intriguingly, and
relevant to the cross-methodology data noted at the
end of their seminal paper, Klüver and Bucy
highlighted striking similarities between primates
following bilateral ATL resection and the patients
previously described by Pick with frontotemporal
dementia. The same pattern as that observed in the
primate studies was replicated in a rare human single-
case neurosurgery study (Terzian & Dalle Ore, 1955).
In an (ultimately unsuccessful) attempt to control the
patient’s epilepsy, these investigators performed
sequential full-depth ATL resections. As in the previ-
ous primate studies, after initial unilateral removal, the
patient exhibited transient deficits of language, recog-
nition. and memory. However, after bilateral resection,
a chronic and severe comprehension deficit emerged,
along with other features of what is now referred to
as Klüver-Bucy syndrome. Taken together, the full
(although admittedly still rather limited) set of neuro-
psychological and neurosurgery findings can be sum-
marized as follows: unilateral ATL damage generates
semantic impairment in the acute stage that often
diminishes rapidly, leaving patients in the chronic
phase with a mild comprehension deficit. This
impairment can be detected with sensitive neuropsy-
chological assessments but is nothing like the level of
semantic impairment found in SD and other bilateral
ATL diseases.
Before considering the explanation for these p0110
findings in more detail, a brief aside to avoid poten-
tial confusion is merited. By far the most famous
example of bilateral temporal resection is that of
patient HM. After surgery, he and the other patients
reported in the seminal case-series study of Scoville
and Milner (Scoville & Milner, 1957) presented with
profound anterograde amnesia but not with other
impairments of higher cognition, including language
and semantic memory. At face value, this might
appear to contradict the hypothesis that semantic
representation is reliant on a bilateral ATL system; in
00061
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61.5 EVIDENCE FOR AND POSSIBLE REASONS FOR A BILATERAL ATL HUB
fact, a closer consideration of the location of the resec-
tions adds further weight to our hypothesis that the
ventrolateral aspects of the ATL are crucial to semantic
memory. Because of the fact that Scoville used an
orbital approach to the medial temporal regions when
performing the bilateral selective hippocampectomy
(rather than the lateral approach commonly used in
most modern neurosurgical procedures), the ventral
and lateral aspects of the ATL were preserved in patient
HM and the other patients in the original case series.
p0115 The notion that both left and right ATL contribute
to semantic representation is reinforced by recent stud-
ies applying rTMS to neurologically intact participants.
The technique is complementary to neuropsychological
studies in that one can assess performance before stim-
ulation and then after it during the transient refractory
period. Its advantage over lesion studies is that the
location and timing of the stimulation are under exper-
imental control; however, the behavioral effect of stim-
ulation is (happily!) not only transient but also much
smaller than that of neurological damage. Careful,
sensitive assessment methods are thus required. As
noted, SD patients always have bilateral temporal
abnormalities, making it difficult in SD to separate and
establish a selective role, if any, of left versus right
ATL. It is possible, however, to contrast the effect of
rTMS to left versus right ATL, and this has been done
for verbal and nonverbal comprehension tasks in a
series of studies (Lambon Ralph, Pobric, & Jafferies,
2009; Pobric et al., 2010a). In these studies, rTMS to
either ATL generated an equivalent effect on both ver-
bal and nonverbal semantic tasks, thus supporting our
working hypothesis that both ATLs contribute to a
transmodal semantic hub.
p0120 A potential explanatory framework for the patient
(SD and unilateral resection) and rTMS results was
explored in a recent computational model of bilateral
ATL semantic representation (Schapiro et al., 2013).
This was based on a direct extension of the original
Rogers “hub-and-spoke” computational model (Rogers
et al., 2004). Instead of a single transmodal representa-
tional hub, however, Schapiro and colleagues split it
into two separate “demi-hubs” with only partial con-
nectivity between them. The model, which was trained
in exactly the same manner as the Rogers single-
hub variant, was able to learn all of the training
patterns despite having a lower number of connec-
tions overall. When considerable unilateral damage
was applied to the simulation, a small semantic
impairment resulted that could be reduced by allow-
ing some postdamage weight adjustment (to mimic
spontaneous recovery; Keidel, Welbourne, & Lambon
Ralph, 2010; Welbourne & Lambon Ralph, 2007;
Welbourne, Woollams, Crisp, & Lambon Ralph, 2011).
In contrast, when the same total amount of damage
K. CONCEPTUAL SEMANTIC KNOWLEDGE
Hickok-1611153 978-0-12-407794-2
9
was distributed across both demi-hubs, a substantial
and considerably greater semantic deficit emerged—
replicating the difference between patients with unilat-
eral versus bilateral ATL lesions. Detailed analysis and
mathematical exploration demonstrated that the differ-
ence between unilateral and bilateral damage in the
model was related to the differential propagation of
noisy activation. Damage in any computational model
not only diminishes the level of activation but also
adds noise to its processing. When damage is focussed
within one (only partly interconnected) demi-hub, the
unaffected system generates strong and relatively
noise-free activations that are able to dominate the
response from the model; thus, it performs generally
accurately (albeit slightly less efficiently than before).
In contrast, bilateral damage across both demi-hubs
results in weakened and noisy representations, leading
to inaccurate responses.
Although it seems clear that both left and right p0125
ATLs are important to conceptual knowledge, the cur-
rent literature contains mixed results and conclusions
regarding the nature of the contribution from each
side. Based on results from a variety of techniques,
some researchers argue for a left right dissociation
in which the left ATL is primarily responsible for ver-
bal semantic processing, whereas the right is much
more important in processing faces, objects, and non-
verbal sounds (Gainotti, 2012, 2014; Mesulam et al.,
2013; Snowden, Thompson, & Neary, 2004; Thierry &
Price, 2006). Other research groups report results
more compatible with either similar contributions from
the two ATL sides or at least only graded dissocia-
tions. Furthermore, even results indicating left right
dissociation are open to a different and more subtle
interpretation than a categorical “left 5 verbal, right 5
nonverbal.” There is no doubt that cortical regions
posterior to the ATL have significantly different
involvement in the processing of verbal versus nonver-
bal information. Given that the great majority of corti-
cocortical connections are very local and within rather
than across the hemisphere, this means that as infor-
mation moves from caudal (sensory) regions to rostral
(conceptual) regions, verbal input will activate the left
ATL more than the right, and nonverbal input such as
faces and objects will preferentially activate the right
ATL. This account of left/right differences in semantic
processing, including two implemented computational
models, has been advanced by Ikeda, Patterson,
Graham, Lambon Ralph, and Hodges (2006), Lambon
Ralph, McClelland, Patterson, Galton, and Hodges
(2001), Mion et al. (2010), and Schapiro et al. (2013).
In conclusion, the current literature provides only a p0130
partial answer to the nature of the contribution of left
versus right ATL to semantic processing. There is
broad agreement (across methods and patient groups)
00061
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10 61. THE HUB-AND-SPOKE HYPOTHESIS OF SEMANTIC MEMORY
that both left and right ATL contribute in some fashion
and that the left ATL is more involved than the right
in generating names and speech from semantic
memory. The issues that are subject to considerable
current research activity center around two alternative
hypotheses: (i) graded connectivity-related differences
in the contribution of each ATL to a primarily bilateral
neural system or (ii) a more modular distinction in
which each ATL is relatively specialized for discrete
subdivisions of semantic processing.
s0035
61.6 THE GRADED HUB HYPOTHESIS
p0135 In this final section, we consider potential functional
variations within each ATL. As noted, although the
robust and consistent data from SD patients have been
crucial in linking bilateral ATLs to semantic represen-
tation, these findings are a less powerful source of
information regarding the contributions of left versus
right ATL. In a similar vein, although the atrophy in
SD is generally agreed to be more profound in the ven-
tral than the dorsal ATL, most of the ATL is abnormal
by the time that SD patients come to clinical attention,
with the result that the condition of SD is insufficient
to inform us about potential variations in representa-
tion of conceptual knowledge from dorsal to ventral
regions. There is also the question of lateral versus
medial aspects of the ATL. All of these “unknowns”
constitute yet another reason for adopting multiple
methods, because limitations in one approach can
often be compensated by advantages conferred by
other techniques.
p0140 Ever since the seminal work of Brodmann (1909), it
has been known that there are variations in cyto-
architecture that, in turn, imply different types of
neurocomputation. Two major distinctions in the ATL
region noted by Brodmann were a shift from granular
through dysgranular to agranular cortex in moving
from lateral to medial structures around the temporal
pole and a significant change in cytoarchitecture from
BA22 (approximately equivalent to the superior tem-
poral gyrus) to the neighboring areas (pole, BA38;
middle and inferior temporal gyri, BA21 and BA20,
respectively). Although noting that there were also
differences between the other ATL regions (sufficient
to give them different labels), Brodmann commented
that they were graded rather than absolute differences;
in fact, it is possible to consider them to be one single
larger cytoarchitectural region as some of his contem-
poraries did. Modern, sophisticated studies (Ding, Van
Hoesen, Cassell, & Poremba, 2009) have increased the
number of cytoarchitectural divisions proposed for the
ATL but, echoing Brodmann’s original observations,
these divisions are thought to be graded rather than
K. CONCEPTUAL SEMANTIC KNOWLEDGE
Hickok-1611153 978-0-12-407794-2
absolute in nature. Although local cytoarchitecture
is only one factor in neurocomputation (others—like
connectivity—are also crucial), these classic and con-
temporary findings might lead us to expect some func-
tional variations across the ATL, albeit they are
probably graded in nature.
Recent (distortion-corrected) neuroimaging studies p0145
have provided new insights about white-matter con-
nectivity within the ATL and also the location of
semantically related functional activations. With
regard to white-matter connectivity, Binney et al.
(2012) observed connections both along gyri and
between neighboring gyri, providing a neural basis for
blending of information in a rostral and lateral direc-
tion along the temporal cortex. In addition, there is a
more regionally specific pattern of connectivity from
the temporal lobe to other areas. The temporopolar
cortex is primarily connected via the uncinate fascicu-
lus to orbitofrontal and ventral prefrontal regions, pos-
terior temporal areas to inferior parietal regions, and
superior temporal areas to inferior prefrontal regions.
Very similar patterns of connectivity have been
revealed by a recent analysis of resting-state functional
connectivity seeded from different parts of the human
temporopolar cortex (Pascual et al., 2013). These long-
range connections are likely to be germane not only for
considering how various forms of modality-specific
information interact with a transmodal ATL hub but
also for considering how semantic representations
interface with other cognitive mechanisms, such as
executive functions and working memory (Binney
et al., 2012; Jefferies & Lambon Ralph, 2006).
With the benefit of methods and techniques to allow p0150
effective probing of activations across the entire ATL
(including ventral regions), recent fMRI studies have
started to reveal various graded patterns of semantic
activation, which seem to fit with the graded differences
in connectivity and cytoarchitecture in this area (Binney
et al., 2012; Ding et al., 2009). These neuroimaging stud-
ies point to the bilateral ventrolateral subregion as the
centerpoint of a graded ATL semantic hub. Across stud-
ies, this region is consistently activated, irrespective of
task, input modality, or category of stimuli (Sharp et al.,
2004; Vandenberghe et al., 1996; Visser et al., 2012;
Visser & Lambon Ralph, 2011). Moving away from
this neural location, there seem to be gradual shifts in
the semantic function dependent on the proximity/
connectivity to different primary inputs (Visser et al.,
2012; Visser & Lambon Ralph, 2011). Thus, activation is
more sensitive to auditory-related stimuli (verbal and
nonverbal) in lateral superior regions and to visual
inputs in posterior ventral temporal areas. These early
explorations of the ATL region are consistent with
variants of the hub-and-spoke model that include
graded variations of connectivity (Plaut, 2002).
00061
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REFERENCES
p0155 In summary, recent evidence has made it clear that
the ATL does not function as one undifferentiated
mass but rather with important graded variations of
function across the region. Given the pattern of its
structural and functional connectivity, these graded
changes in ATL function appear to reflect the varying
influence of different inputs and outputs on the
processing in local ATL subregions.
s0040
61.7 CONCLUDING COMMENT
p0160 Semantic memory/conceptual knowledge is central
to much of human life. It may not be involved when
you walk into a room to sit down, but recognizing that
an unfamiliar chair is something on which to sit
requires semantic memory. It may not be involved
when you move your tongue and lips, but it is the basis
of every novel utterance that you make. A huge amount
has been learned about this central aspect of human
function in the relatively short time in which cognitive
neuroscientists have been addressing it in their experi-
mental work and theorizing, but there is so far to go
that future models of the organization and neural basis
of semantic memory may look like “objects” that we
have never encountered before. It would be a foolhardy
researcher who tries to predict which of the field’s
current interpretations of data will still be alive one or
several decades from now. Maybe the proposal of a
semantic hub will be here today and gone tomorrow.
All we can say is that today, we find it difficult to con-
ceive of a hub-less framework that would account for
existing data regarding semantic memory.
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 To protect the rights of the author(s) and publisher we inform you that this PDF is an uncorrected proof for internal business use only by the author(s), editor(s), reviewer(s), Elsevier
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NON-PRINT ITEM

Abstract
Semantic memory represents our knowledge about the meanings of words, objects, people, and all other ver-
bal and nonverbal stimuli that we encounter in the world. The semantic network in the human brain encodes all
of this information, reactivates it rapidly and effortlessly, and generalizes appropriately across different exem-
plars and situations to form coherent concepts. This chapter considers how coherent concepts are formed and
argues that the semantic network must include both modality-specific primary and association areas and a cru-
cial transmodal hub. Drawing on evidence from normal and disrupted semantic processing, we consider the
growing evidence that regions in the anterior temporal lobe (ATL) are the foundation of this representational
hub and assess the possible roles of left versus right and dorsal to ventral ATL subregions.
Keywords: Anterior temporal lobe; semantic dementia; hemispheric differences; embodied cognition; transcranial
magnetic stimulation

Hickok-1611153 978-0-12-407794-2 00061

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