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焦点功能:
Biomarkers in Network Neuroscience

Multimodal connectome biomarkers of
cognitive and affective dysfunction
in the common epilepsies

Raul Rodriguez-Cruces1*, Jessica Royer1*, Sara Larivière1, Dani S. Bassett2,3,4,5,6,7,
Lorenzo Caciagli2,8*, and Boris C. Bernhardt1*

1McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, 麦吉尔大学, 蒙特利尔, Quebec, 加拿大
2Department of Bioengineering, 宾夕法尼亚大学, 费城, PA, 美国
3Department of Physics and Astronomy, 宾夕法尼亚大学, 费城, PA, 美国
4Department of Electrical and Systems Engineering, 宾夕法尼亚大学, 费城, PA, 美国
5神经内科, 宾夕法尼亚大学, 费城, PA, 美国
6Department of Psychiatry, 宾夕法尼亚大学, 费城, PA, 美国
7Santa Fe Institute, 圣达菲, NM, 美国
8Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, 伦敦, 英国
*Denotes equal contribution.

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关键词: Epilepsy, 认识, Affect, Dysfunction, Connectomics, Neuroimaging, 网络
神经科学

抽象的

Epilepsy is one of the most common chronic neurological conditions, traditionally defined as a
disorder of recurrent seizures. Cognitive and affective dysfunction are increasingly recognized as
core disease dimensions and can affect patient well-being, sometimes more than the seizures
他们自己. Connectome-based approaches hold immense promise for revealing mechanisms
that contribute to dysfunction and to identify biomarkers. Our review discusses emerging
multimodal neuroimaging and connectomics studies that highlight network substrates of
cognitive/affective dysfunction in the common epilepsies. We first discuss work in drug-resistant
epilepsy syndromes, 那是, temporal lobe epilepsy, related to mesiotemporal sclerosis (TLE), 和
extratemporal epilepsy (ETE), related to malformations of cortical development. While these are
traditionally conceptualized as ‘focal’ epilepsies, many patients present with broad structural and
functional anomalies. 而且, the extent of distributed changes contributes to difficulties in
multiple cognitive domains as well as affective-behavioral challenges. We also review work in
idiopathic generalized epilepsy (IGE), a subset of generalized epilepsy syndromes that involve
subcortico-cortical circuits. 全面的, neuroimaging and network neuroscience studies
point to both shared and syndrome-specific connectome signatures of dysfunction
across TLE, ETE, and IGE. 最后, we point to current gaps in the literature and formulate
recommendations for future research.

作者总结

Epilepsy is increasingly recognized as a network disorder characterized by recurrent seizures
as well as broad-ranging cognitive difficulties and affective dysfunction. Our manuscript
reviews recent literature highlighting brain network substrates of cognitive and affective
dysfunction in common epilepsy syndromes, namely temporal lobe epilepsy secondary to

开放访问

杂志

引文: Rodriguez-Cruces, R。, Royer,
J。, Larivière, S。, Bassett, D. S。, Caciagli,
L。, & Bernhardt, 乙. C. (2022).
Multimodal connectome biomarkers of
cognitive and affective dysfunction in
the common epilepsies. 网络
神经科学, 6(2), 320–338. https://土井
.org/10.1162/netn_a_00237

DOI:
https://doi.org/10.1162/netn_a_00237

已收到: 1 十月 2021
公认: 2 二月 2022

利益争夺: 作者有
声明不存在竞争利益
存在.

通讯作者:
Boris C. Bernhardt
boris.bernhardt@mcgill.ca

处理编辑器:
Mario Senden

版权: © 2022
麻省理工学院
在知识共享下发布
归因 4.0 国际的
(抄送 4.0) 执照

麻省理工学院出版社

Connectome biomarkers of cognitive/affective dysfunction in epilepsy

mesiotemporal sclerosis, extratemporal epilepsy secondary to malformations of cortical
发展, and idiopathic generalized epilepsy syndromes arising from subcortico-cortical
pathophysiology. We discuss prior work that has indicated both shared and distinct brain
network signatures of cognitive and affective dysfunction across the epilepsy spectrum,
improves our knowledge of structure-function links and interindividual heterogeneity, 和
ultimately aids screening and monitoring of therapeutic strategies.

介绍

Epilepsy is a neurological disorder characterized by recurrent seizures, affecting around 1% 的
世界人口 (大约 50 百万人) (GBD 2016 Neurology Collaborators,
2019). While seizures can be controlled with antiseizure medications in most patients, 30–
40% of individuals are drug resistant and are at higher risk of widespread and cumulative brain
damage (Bernasconi & Bernhardt, 2010; Bernhardt et al., 2009乙, 2013乙; Caciagli et al., 2017;
Coan et al., 2009; Galovic et al., 2019). 而且, cognitive impairment has been reported to
encompass multiple domains (Loring et al., 2004), including memory, executive function, 和
language abilities. Difficulties in mood and emotion regulation are also increasingly recog-
尼泽德, challenging patient well-being and quality of life (Bell et al., 2011; Hermann et al.,
2009). Collectively, these findings underscore the broad impact of epilepsy on brain health
and function and emphasize the importance of shifting our understanding and clinical man-
agement of epilepsy as a disorder characterized by more than seizures (Selassie et al., 2014).

Temporal lobe epilepsy (TLE) related to mesiotemporal sclerosis as well as extratemporal
epilepsy (ETE) related to malformations of cortical development are among the most common
drug-resistant epilepsy syndromes. While both TLE and ETE have been traditionally labeled as
‘focal’ epilepsies related to a confined brain region, they are increasingly understood as
system-level disorders of interconnected networks (Gleichgerrcht et al., 2015; Larivière
等人。, 2021; Tavakol et al., 2019). A growing body of neuroimaging as well as histopatholo-
gical findings demonstrates diffuse network anomalies in both syndromes, affecting regions
beyond the area responsible for the onset of seizures (Bernhardt et al., 2013A, 2015; Caciagli
等人。, 2014). 而且, emerging work combining neuroimaging and cognitive testing
suggests clear associations between atypical brain connectivity and measures of cognitive as
well as affective function. Idiopathic generalized epilepsies (IGE), 另一方面, constitute
大约 20% of all patients with epilepsy and include childhood absence epilepsy,
juvenile absence epilepsy, juvenile myoclonic epilepsy, and epilepsy with generalized
tonic-clonic seizures alone. Neuroimaging studies in IGE have detected widespread anomalies
in brain structure, 连接性, and function—paralleling mounting evidence in TLE and ETE
on system-level dysfunction. 此外, multiple studies assessing cognitive abilities point to
syndrome-specific impairments with, 例如, measurable deficits in executive function as
well as social and affective disturbances in patients with juvenile myoclonic epilepsy, 和
visuospatial and language deficits in absence epilepsies (Ratcliffe et al., 2020; Guida et al.,
2019). Collectively, these studies suggest that widespread network anomalies contribute not
only to the clinical manifestations of the disease, such as seizure burden and treatment
response, but also to cognitive and affective difficulties affecting many patients’ lives.

Advances in multimodal neuroimaging and connectome analysis have contributed to our
growing understanding of the structural and functional organization of brain networks
(Larivière et al., 2018) and promise to provide candidate metrics that could inform clinical care
(Larivière et al., 2021). In this targeted review, we will survey recent literature assessing

Epilepsy:
A common chronic condition
characterized by recurrent seizures.

TLE:
Temporal lobe epilepsy, one of the
most common epilepsy syndromes
and one that is often drug-resistant.

Mesiotemporal sclerosis:
A lesion characterized by cell loss
and/or gliosis of the mesiotemporal
lobe structures, 例如
hippocampus and entorhinal cortex,
common in patients with TLE.

ETE:
Extratemporal lobe epilepsy, A
heterogenous group of epilepsy
syndromes characterized by
seizures originating from outside
the temporal lobes.

Malformations of cortical
发展:
A spectrum of lesions associated with
atypical cortical development and
a frequent cause of drug-resistant
seizures.

IGE:
Idiopathic generalized epilepsy, A
group of epilepsy syndromes
associated to generalized seizures
that are believed to have a strong
polygenetic basis.

Connectome:
A systematic representation of the
brain’s network (either structural or
functional).

网络神经科学

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

Biomarker:
An objectively measured indicator of
a biological process, normal or
pathological, with potential
diagnostic or prognostic utility for a
given person/patient.

connectome biomarkers of cognitive and affective dysfunction across common epilepsy syn-
dromes, notably TLE, ETE, and IGE. 具体来说, we will discuss the current literature on struc-
tural and functional network anomalies in each of these syndromes, outline the prevailing
notions of syndrome-related cognitive dysfunction, and summarize emerging literature relating
network neuroscience findings to neuropsychological assessments. 全面的, findings support
both shared and syndrome-specific patterns of structural and functional brain network reor-
ganization across different spatial scales, motivating an integrative approach combining
multidimensional behavioral phenotyping, multimodal neuroimaging, 和, 理想地, the in-
clusion of a spectrum of epilepsy syndromes (数字 1). To conclude, we will highlight gaps in
the literature and make recommendations for future research on brain and cognition in the
common epilepsies.

TEMPORAL LOBE EPILEPSY

The most common and widely studied drug-resistant epilepsy in adults is temporal lobe epi-
lepsy (TLE). This syndrome is traditionally associated with variable degrees of histopatholo-
gical alterations within mesial temporal lobe structures, such as the hippocampus, amygdala,
and entorhinal cortex (Blumcke et al., 2013; Thom, 2014; Thom et al., 2009). Mounting his-
topathological and neuroimaging literature, 然而, challenges the notion that the condition
can be reduced to localized pathology in the mesiotemporal lobes. Histological data suggests
that mesiotemporal alterations often co-occur with broad rearrangements of cortical

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Investigating cognitive and affective dysfunction across the common epilepsies requires an integrative approach, combining mul-
数字 1.
tidimensional behavioral phenotyping, multimodal neuroimaging, 和, 理想地, the inclusion of a spectrum of epilepsy syndromes. In the cur-
rent review, we summarize the literature that has so far populated this space in temporal lobe epilepsy (TLE), extratemporal epilepsy (ETE), 和
idiopathic generalized epilepsy (IGE).

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

MRI:
Magnetic resonance imaging.

建筑学, together with cell loss and gliosis in temporal and extratemporal cortices as well
as subcortical structures, particularly the thalamus (Blanc et al., 2011; Margerison & Corsellis,
1966). These findings have been confirmed in vivo, based on structural MRI assessments
applying volumetric analysis, as well as with automated surface-based measures (Bernhardt
等人。, 2008, 2012, 2015, 2016; 林等人。, 2007; McDonald et al., 2008). These studies have
报道, in both single and multisite datasets, that TLE is often associated with diffuse cortical
atrophy affecting mesiotemporal, lateral temporal, frontal, and centroparietal cortices, 还有
as profound atrophy of several subcortical structures (Larivière et al., 2020A; Whelan et al.,
2018). While the distribution of gray matter atrophy appears relatively widespread and
bilateral, analysis of cortical asymmetries has pointed more directly to marked changes in ipsi-
lateral structures, particularly in temporo-limbic regions. These findings have been complemen-
ted by quantitative analysis of other MRI contrasts, such as FLAIR/T2w imaging (Adler et al.,
2018) as well as quantitative T1 relaxometry (Bernhardt et al., 2018), suggesting that structural
alterations are broad, yet most concentrated in paralimbic areas ipsilateral to the seizure
focus. 相似地, several diffusion MRI studies have described anomalies in structural con-
nectivity and subcortical white matter microstructure, strongly affecting temporo-limbic
pathways and with more moderate effect sizes in extralimbic collateral and commissural
pathways (Concha et al., 2005, 2009, 2012; Focke et al., 2008; 刘等人。, 2016). 分析
of brain function and connectivity, as measured by task-based and resting-state fMRI, 有
shown atypical functional interactions between temporal and extratemporal areas in TLE
patients relative to controls, with most marked findings in temporo-limbic and default
mode networks, systems known to be anatomically connected to the mesiotemporal lobe
(Bernhardt et al., 2016; Larivière et al., 2020乙). 全面的, despite sometimes diverging
topographies of regional changes across different neuroimaging modalities, findings con-
verge toward widespread network reorganization in TLE, likely modulated by anatomical
connections to a mesiotemporal/paralimbic disease epicenter.

Considering cognitive function, a majority of TLE patients has traditionally been reported to
show memory impairment, while around 30%–40% present with difficulties in language func-
的 (Reyes et al., 2018). Paralleling the widespread anomalies revealed by neuroimaging and
histology, an increasing body of work suggests that impairments in executive (Lutz &
Helmstaedter, 2005), 感官的, and motor functions are also prevalent in TLE (Hermann et al.,
2009; 林等人。, 2012; McAndrews & Cohn, 2012; Saling, 2009). 像这样, the landscape of
cognitive difficulties in TLE emphasizes a broad profile of impairments across patients affecting
multiple cognitive domains. Adding to the complexity of the cognitive dysfunction landscape
in TLE, impairments are also quite variable across patients. Several groups have previously
suggested the existence of graded abnormalities across TLE patient subgroups, with approxi-
mately a third of patients presenting with marked dysfunction while the remaining patients
show mild or no measurable impairments compared to age-matched healthy individuals
(Rodriguez-Cruces et al., 2018). In TLE, the degree and laterality of structural pathology in
the hippocampus have been associated with verbal memory and language impairments, 和
patients with left sided and more marked pathology showing greater impairment (Dabbs et al.,
2009; Stewart et al., 2009). 此外, functional connectivity measures of the hippocam-
pus and cortical networks have been used to probe language lateralization (Benjamin et al.,
2017; Berl et al., 2013; Lopes et al., 2019) and to predict deficits in episodic memory (李等人。,
2021). In the latter study, the investigators reported an atypical organization of functional con-
nections that link the hippocampus to widespread cortical areas; the data suggests that the
structural reorganization of the hippocampus and its functional interactions with the rest of
the brain underpins reorganization of memory networks toward a potentially less efficient

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

functional architecture (李等人。, 2021). Such findings are in line with earlier fMRI findings in
TLE patients during memory tasks, showing a reorganization of both ipsilateral and contralat-
eral hippocampal and extrahippocampal functional networks (Alessio et al., 2013; Bigras
等人。, 2013; Jokeit et al., 2001; Sidhu et al., 2013). Other work studied intrinsic functional
hubs in TLE and reported an association between functional network reorganization and both
language and memory impairment in patients (Roger et al., 2020). 一起, these studies
emphasize the role of (1) hippocampal-neocortical subnetworks and (2) structural alterations
in the mesiotemporal lobes in determining cognitive deficits in TLE, particularly relating to
memory and language function.

A separate and complementary series of studies identified associations between structural
connectivity measures and cognitive phenotypes in TLE. There has been robust evidence for
an association between diffusion abnormalities of deep white matter fiber tracts as well as the
superficial white matter, and reduced language and memory performance in patients (Reyes
等人。, 2019). In one study, the authors combined dimensional and categorical multivariate
approaches to show that more marked degrees of impairment across several cognitive func-
tions related to overall less efficient and less interconnected white matter network organization
(数字 2, top left) (Rodriguez-Cruces et al., 2019). Another study leveraged communication
型号, which simulate functional interactions from structural connectivity data, and reported
that overall delays in regional interactions related to broad impairments in several cognitive
域 (Girardi-Schappo et al., 2021). Moving toward a biomarker evaluation framework,
connectome-based machine learning—with cross-validation and the use of an independent
hold-out dataset—has shown utility in predicting memory and language impairment, demon-
strating outlook that brain network models can aid in indexing patient-specific functional
impairments (Balachandra et al., 2020; Kaestner et al., 2020). In one of these studies, 结构性的
connectivity features achieved improved performance when they were combined with hippo-
campal imaging features, pointing to benefits of combining targeted assessments of the mesio-
temporal epicenter with large-scale network models (Balachandra et al., 2020). 因此, 这
above studies emphasize the importance of efficient network communication in preserving
cognition in TLE patients, and hold promise as robust biomarkers of cognitive difficulties in
this population.

A growing body of studies, including combined phenotyping and neuroimaging efforts such
as the Epilepsy Connectome Project, also assessed the utility of resting-state fMRI connectivity
measures in the study of cognitive dysfunction in TLE. Combining resting-state fMRI connec-
tivity analysis, morphological assessment, and supervised machine learning, a previous study
assessed structural and functional brain aging in TLE patients, and reported associations
between accelerated aging and cognitive decline in patients, particularly with regard to fluid
能力 (Hwang et al., 2020). These findings are paralleled by reports of regional and global
alterations in intrinsic functional network organization in TLE, showing associations between
network alteration in the temporal lobe and clinical measures on the one hand, and global
network clustering and cognitive decline on the other hand (Struck et al., 2021). 其他
recent study leveraged stepwise functional connectivity analysis, an approach tapping into
putative cortical hierarchical organization, and showed associations between atypical
sensory-fugal and hippocampo-cortical organization in TLE and cognitive dysfunction across
multiple domains (数字 2, top right) (Fadaie et al., 2021). Several studies have furthermore
used resting-state fMRI to examine functional connectivity changes between brainstem nuclei
of the ascending arousal system as well as cortical and subcortical regions (Englot et al., 2017,
2018). The authors reported overall reduced connectivity in patients, which reflected an
increased frequency of seizures with impaired awareness and disease severity measures,

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

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数字 2. Prior multimodal imaging studies on connectome markers of dysfunction in the common epilepsies. In temporal lobe epilepsy (TLE;
top row), structural network measures were related to cognitive dysfunction across multiple domains (top left) (Rodriguez-Cruces et al., 2019).
Using stepwise functional connectivity analysis, alterations in hierarchical functional network organization were shown to reflect multidomain
cognitive impairment (top right) (Fadaie et al., 2021). In extratemporal epilepsy (ETE; middle row), a study focusing on children with frontal
lobe seizures demonstrated that despite the absence of significant differences in structural network parameters in patients, structural modularity
increased with more marked cognitive impairment (middle left) (Vaessen et al., 2014) . When comparing fMRI activation patterns in a verbal
working memory task, frontal lobe epilepsy patients showed targeted reductions in the recruitment of specific networks, notably fronto-parietal
and dorsal attention systems, while effects in TLE patients were more widespread (middle right) (Caciagli et al., 2022). As for idiopathic gen-
eralized epilepsy syndromes (IGE; bottom row), a study in patients with juvenile myoclonic epilepsy and their unaffected siblings investigated
left hippocampal shape/positional anomalies and found associations to atypical activation during a verbal memory task (bottom left) (Caciagli
等人。, 2019). Enhanced recruitment of motor systems during cognitive tasks, construed as an imaging phenotype in both patients and their
unaffected siblings, was seen when assessing both memory and language tasks combined (bottom right) (Caciagli et al., 2020).

alongside with impairments in verbal IQ, 注意力, executive function, 语言, and visuo-
spatial memory (Englot et al., 2017, 2018). These findings in part recapitulate experimental
work in animal models that have suggested an implication of subcortico-cortical loops in
TLE pathophysiology and functional impairment. By using deep brain stimulation of specific

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

thalamic divisions in animal models, it was demonstrated that cortical slow-wave activity can
be reduced, which could also lead to reduced postictal behavioral impairment, supporting a
potential therapeutic value of modulating subcortico-cortical loops (徐等人。, 2020).

Cognitive dysfunction may co-occur with socio-affective difficulties. A substantial propor-
tion of patients suffer from depressive symptoms, anxiety, and personality disorders (Kanner
等人。, 2012; Tellez-Zenteno et al., 2007). As for cognitive dysfunction, affective symptoms
may have a considerable impact on patient well-being and quality of life. In one previous
学习, the investigators related self-reports from the Beck Depression Inventory to structural
and functional connectivity measures in both TLE patients and controls (陈等人。, 2012;
Kemmotsu et al., 2013). The authors observed that structural and functional organization of
fronto-limbic circuits, particularly connectivity between the hippocampus and anterior frontal
地区, was associated with depressive symptoms. Fronto-limbic involvement was also sug-
gested by one study relating resting-state fMRI connectivity measures to measures of neurot-
icism, depression, and anxiety (Doucet et al., 2013). The authors showed that neuroticism, A
personality trait that is associated with depressive symptoms relates to atypical functional
connectivity between mesiotemporal and frontal lobe regions, with connectivity alterations
that were partially overlapping to those related to depression and anxiety symptoms (Rivera
Bonet et al., 2020). In an earlier study, the authors also reported associations between affec-
tive symptoms and reductions in gray matter volumes, again targeting both frontal and tem-
poral neocortices, as well as mesiotemporal lobe structures such as the hippocampus and
amygdala (Rivera Bonet et al., 2019). Collectively, previous efforts to study socio-affective
functioning in TLE highlight the role of fronto-limbic circuits, as well as the structural integ-
rity of these regions, in mood-related symptoms.

EXTRATEMPORAL LOBE EPILEPSY

Extratemporal lobe epilepsy (ETE) refers to a broad class of location-related syndromes in
which the seizures originate from regions outside of the temporal lobe. The most common
ETE subsyndrome is frontal lobe epilepsy, which accounts for approximately 50% of ETE
患者 (Delev et al., 2019; 李等人。, 2008). Although lesional etiologies are quite variable
in ETE, many patients present with a suspected or histologically confirmed malformation of
cortical development, such as focal cortical dysplasia (type-1 or type-2), heterotopia (subcor-
tical nodular, 乐队), or polymicrogyria. Some of these lesions may be subtle and overlooked
upon conventional radiological examination, contributing to diagnostic uncertainty and diffi-
culties in offering targeted surgical therapy (Bernasconi et al., 2011; Bernasconi & Bernasconi,
2011). While significant effort has been invested in characterizing malformations in single
patients by using structural MRI and, 日益, connectomics techniques (Bernasconi
等人。, 2001; Colliot et al., 2005; S. Hong et al., 2017A, 2017乙; 王等人。, 2015), 最近的
studies have also characterized the whole-brain substrates of ETE cohorts at a group level.
These studies have shown that structural and functional network substrates across different
ETE subsyndromes likely vary with respect to the primary lesional etiology. Patients with
type-1 focal cortical dysplasia (a late-stage malformation associated with subtle alterations
in cortical architecture and intensity) present with widespread cortical thinning relative to
controls. 相比之下, patients with type-2 dysplasia (early-stage cortical malformations that
manifest on MRI as cortical thickening and interface blurring, together with FLAIR/T2w inten-
sity changes; Hong et al., 2014, 2015) present with patches of increased cortical thickness
beyond the primary lesional perimeter (Hong et al., 2016). A previous network analysis of
frontal lobe epilepsy patients with different cortical malformations revealed a gradient of
functional and structural network anomalies, showing only subtle structural network

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

reorganization in type-2 dysplasia, moderate effects in heterotopias, and maximal changes in
late-stage malformations such as polymicrogyria (Hong et al., 2017A). Findings were paralleled
by graded functional network anomalies, pointing to reductions in functional network effi-
ciency across the malformation spectrum, again being more pronounced in late-stage cortical
malformations such as polymicrogyria than in early-stage proliferative etiologies such as type-
2 dysplasia (Hong et al., 2017A). Previous work on ETE, 因此, emphasizes the importance of
considering the developmental etiology of lesional subtypes to understand structural and func-
tional network anomalies in specific patient subgroups.

In ETE, the landscape of cognitive impairment is less well characterized than in TLE, owing
to heterogeneity of the patients’ primary etiology and variable extent of the epileptogenic net-
工作. Findings nevertheless suggest a modulation of impairments with respect to the location
of the disease epicenter. 例如, ETE patients with a suspected or confirmed anomaly in
the frontal lobes will often present with executive dysfunction (Braakman et al., 2011; Exner
等人。, 2002; Patrikelis et al., 2016; Upton & 汤普森, 1996; Verche et al., 2018), 测距
from impaired attention to difficulties in goal-oriented behaviors. Verbal competencies also
appear impaired (Helmstaedter et al., 1996; Risse, 2006), and reports have pointed to poorer
motor coordination and reduced psychomotor speed (Upton & 汤普森, 1996, 1997).
Patients with lesions in central and posterior regions may show deficits in visuospatial func-
系统蒸发散, often together with attentional and motor dysfunction. Similar heterogeneity exists even
within subgroups of patients with the same lesional subtype, where deficits can range from no
apparent cognitive impairment to marked disability.

Studies assessing brain substrates of cognitive deficits in patients with ETE are less frequent
than in TLE and are also more difficult to aggregate due to the above-mentioned heterogeneity
across the patient spectrum. 然而, prior work in ETE samples (sometimes mixed with TLE)
reported structural and functional connectivity alterations that relate to overall reductions in
cognitive function (Vaessen et al., 2012, 2013). In mixed focal epilepsy cohorts including
patients with ETE, prior work highlighted frontotemporal connectivity abnormalities and global
alterations of functional network architecture during language tasks (Vlooswijk et al., 2010,
2011A), and prefrontal connectional rearrangements during verbal working memory
(Vlooswijk et al., 2011乙). In children with frontal lobe epilepsy, recent studies showed altered
functional connectivity among fronto-temporo-parietal cortices during a working memory task
compared to controls (Braakman et al., 2013), and also reported an association between atyp-
ical functional network modularity, consisting of reduced long-range connectivity and
increased short-range connections, and reductions in cognitive performance (Vaessen et al.,
2013). 尤其, associations between cognitive impairment and network topology have been
reported in structure as well as function. 例如, structural networks estimated from dif-
fusion MRI tractography evince marked alterations in segregation and integration in patients
with more severe cognitive impairment (数字 2, middle left) (Vaessen et al., 2012); similarly,
increased clustering in structural covariance networks derived from T1-weighted data was not
only associated with markers of disease severity but also with lower general intelligence
(Drenthen et al., 2018). In a recent study, we combined a comprehensive cognitive profiling
of language and working memory abilities with task-based fMRI analysis and connectome-
level contextualization in a cohort with frontal lobe epilepsy, and compared findings to both
patients with TLE and healthy controls (数字 2, middle right) (Caciagli et al., 2022). 我们的
study showed that working memory and language impairment in frontal lobe epilepsy was
associated with reduced activation across attentional and executive systems, together with
an attenuated deactivation of default mode regions, suggesting a reorganization of functional
recruitment at the systems level. While atypical activation patterns were similar to those in TLE

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

患者, reductions in default mode network deactivations appeared more marked in frontal
lobe epilepsy patients, whereas those with TLE presented with less activations in posterior lan-
guage areas during semantic tasks (Caciagli et al., 2022). Collectively, these findings provide
emerging evidence of both shared and syndrome-specific impacts of different location-related
epilepsies on brain functional networks. 而且, this work broadly illustrates the utility of
network neuroscience approaches in capturing important substrates that contribute to interpa-
tient variability in cognitive dysfunction.

Studies of socio-affective functioning are less common than studies of cognitive function in
ETE, but represent an important and growing area of research. One previous study in a cohort
的 40 frontal lobe epilepsy cases reported that 25% have elevated anxiety scores, 40% 有
either elevated depression or elevated anxiety scores, 和 25% have depression scores above
the clinical cutoff (Tang et al., 2012). These values appear higher than in patients with
generalized epilepsies (Tang et al., 2012), but are not as high as those observed in TLE
(Helmstaedter, 2001). 此外, prior work highlights that executive dysfunction in frontal
lobe epilepsy can co-occur with reduced response inhibition, hyperactivity, 痴迷, 和
addictive behaviors that may interfere with overall adaptation to everyday life (Helmstaedter,
2001). While there is abundant literature on behavioral and emotional difficulties in patients
with specific lesions, including foundational case studies in patients with frontal lobe lesions,
有, 据我们所知, no systematic assessments of the relationship between whole-
brain connectome architecture and affective difficulties in ETE patients.

IDIOPATHIC/GENETIC GENERALIZED EPILEPSY

Idiopathic generalized epilepsy (IGE) refers to a group of epilepsy syndromes with likely poly-
genetic inheritance, and characterized by generalized spike and slow-wave discharges on
EEG. While multiple syndromes are subsumed under the umbrella term of IGE (Andermann
& Berkovic, 2001; International League Against Epilepsy, 1989; 诺德利, 2005), converging evi-
dence supports a key role of thalamo-cortical networks (关等人。, 2011). Fronto-thalamo-
cortical involvement during generation and propagation of generalized seizures has been
solidified by electrophysiological work (Blumenfeld, 2003; Gotman et al., 2005). 结构性
MRI studies complemented these findings, by indicating gray matter volume reductions in both
the thalamus and neocortex (Bernhardt et al., 2009A), albeit to a lesser extent than in syn-
dromes such as TLE (Weng et al., 2020; Whelan et al., 2018). In addition to atrophy, recent work
also pointed to atypical cortical folding and cortex-cortical distance relationships in juvenile
myoclonic epilepsy, with the latter also being present in nonaffected siblings (Wandschneider
等人。, 2019). Atypical cortical folding may signify perturbations in underlying brain connec-
系统蒸发散; resting-state fMRI approaches have indeed supported atypical organization of cortico-
thalamic networks in different IGE syndromes, showing aberrant connectivity when seeding
from either cortical or thalamic regions (王等人。, 2011, 2012, 2019). Similar reports have
appeared in diffusion MRI studies, which showed atypical structural connectivity between
thalamic and medial frontal regions in IGE subgroups with juvenile myoclonic epilepsy
( JME) (O’Muircheartaigh et al., 2012).

The cognitive landscape of IGE is also characterized by atypical function across several
域. A systematic review and meta-analysis conducted across 26 studies revealed broad
reductions in cognitive function across multiple domains in IGE patients, involving general-
ized cognitive ability, fluid/crystallized intelligence, processing speed, and memory abilities
(Loughman et al., 2014). Impairments were observed in studies assessing mixed IGE cohorts,
but also when considering specific IGE subsyndromes such as JME, childhood absence

JME:
Juvenile myoclonic epilepsy, A
common generalized epilepsy
syndrome.

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

epilepsies, as well as epilepsy with generalized tonic-clonic seizures alone. Executive dysfunc-
tion represent a common trait across IGE subsyndromes (Ratcliffe et al., 2020), pointing to
frontal lobe involvement, while impairment of visuospatial abilities may generally be subtle
(Loughman et al., 2014). Another review focusing on childhood absence epilepsy also showed
reductions in verbal skills across language and learning tasks, as well as mild impairments in
executive functions (Verrotti et al., 2015). In JME, several studies also point to impaired social
认识 (Guida et al., 2019; Ratcliffe et al., 2020), which may possibly relate to the consis-
tent frontal lobe dysfunction seen in the disorder. Profiles of cognitive difficulties in IGE are
thus seemingly broad, with specific subsyndromes possibly showing more circumscribed
patterns of impairment.

合在一起, studies using cognitive and neuroimaging measures have supported an
overall perturbation in the organization of prefrontal-central-thalamic connections. A posi-
tron emission tomography study reported prefrontal and subcortical glucose hypometabolism
in patients with JME and associations with reduced working memory and mental flexibility
(McDonald et al., 2006). These findings are complemented by a combined structural and
functional MRI study in JME patients and their unaffected siblings, which reported hippo-
campal shape and positional anomalies as well as atypical functional activations, alongside
with associations to impairments in verbal memory (数字 2, bottom left) (Caciagli et al.,
2019). Further task fMRI studies have reported altered motor activation across a battery of
cognitive tasks (数字 2, bottom right) (Caciagli et al., 2020; Vollmar et al., 2011) and atypical
connectivity between prefrontal and motor networks during a working memory paradigm in
both JME patients and their unaffected siblings, supporting that these imaging phenotypes
may constitute heritable traits (Caciagli et al., 2020; Wandschneider et al., 2014). Atypical func-
tional connectivity between prefrontal and thalamic regions was also observed during a verbal
fluency task (O’Muircheartaigh et al., 2012) and was shown to relate to both reduced verbal
fluency and decremented structural connectivity between these regions. Other structural and
diffusion MRI studies in JME also support a network basis for impairment, by underscoring asso-
ciations between gray and white matter alterations in both cortical and thalamic regions and
cognitive impairments in mental flexibility, 语言, and memory function (Caciagli et al.,
2019; Caeyenberghs et al., 2015; O’Muircheartaigh et al., 2011). Compared to the broad liter-
ature on network correlates of dysfunction in JME, association studies between imaging mea-
sures and cognitive variables are less frequent in absence epilepsy (Ratcliffe et al., 2020). 一
study reported atypical cortical morphology and folding in frontal and temporal cortices and
indirectly supported a potential contribution to reductions in verbal and performance IQ mea-
确定 (Tosun et al., 2011). During a sustained attention paradigm, a functional imaging study
revealed an association between lower activation of the medial frontal cortex and impaired
表现, which coexisted with reduction of fronto-insular resting-state connectivity
(Killory et al., 2011). Collectively, although the amount of work associating cognitive pheno-
types with brain network information is more limited for certain IGE subsyndromes, the literature
overall suggests that atypical wiring and cross-talk of thalamic and cortical regions may contrib-
ute to the sometimes rather broad impairments seen in IGE patients.

CONCLUSIONS AND CURRENT GAPS

Neuroimaging and connectomics approaches are beginning to reveal structural, functional,
and network level substrates in TLE, ETE, and IGE. These studies support both shared and
syndrome-specific patterns of cortico-subcortical reorganization across different epilepsy syn-
dromes, with TLE being associated with marked and widespread network reorganization that is

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particularly extensive in the proximity of the mesiotemporal epicenter. While memory and
language deficits are the most commonly reported cognitive difficulties, mounting evidence
suggests that white matter microstructure and functional alterations also contribute to dysfunction
in other cognitive domains, such as executive function. Fronto-limbic alterations in brain structure
and function also contribute to commonly observed affective comorbidities, including depression
and anxiety, and may potentially underpin other traits associated with TLE, such as neuroticism. 在
ETE, neuroimaging and connectomics studies suggest widespread impairments in structural and
functional brain network organization, which seems to be modulated by both location and etiol-
ogy of the primary lesion. 例如, ETE patients with a suspected or confirmed anomaly in
frontal circuits will often present with executive dysfunction as well as reduced verbal com-
petence, sometimes together with poorer motor coordination and reduced psychomotor
速度. Emerging literature has furthermore begun to reveal structural and functional substrates
of cognitive impairments in ETE, suggesting reorganization in multiple brain subnetworks,
often characterized by atypical activation/deactivation patterns of large-scale functional sys-
特姆斯. 最后, although the different syndromes subsumed under the “IGE” umbrella term are
relatively heterogenous, consistent structural and functional imaging findings point to
thalamo-cortical structural and functional dysfunction. Across different IGE syndromes, 最多
work has been performed in JME, pointing to similar, albeit somewhat more subtle cognitive
impairment than in ETE patients with a frontal lobe seizure focus.

It is plausible that brain network measures may ultimately serve as powerful intermediary
phenotypes to study effects of biological as well as environmental factors on cognitive systems
in people with epilepsy, including medication effects, disease status, and baseline genetic fac-
托尔斯. 尤其, genetic influences are increasingly recognized to play a major role in shared and
distinct connectomic and cognitive phenotypic associations across common epileptic syn-
dromes (Busch et al., 2014; Zhu et al., 2020). To obtain a more thorough understanding of
these likely complex interactions, future studies are recommended that combine multimodal
imaging and connectomics with genetic testing as well as rigorous clinical phenotyping, 在
order to obtain a comprehensive picture of mechanisms leading to cognitive and affective
dysfunction.

By offering a more comprehensive characterization of whole-brain alterations, incorpora-
tion of brain network fingerprinting could possibly aid in the calibration and monitoring of
therapeutic efforts in patients with epilepsy. As this review has outlined, brain network
measures have been repeatedly shown to reflect interindividual differences in cognitive
impairment in different epilepsy syndromes (Balachandra et al., 2020; Hermann et al.,
2020; Kaestner et al., 2020; Reyes et al., 2019; Rodriguez-Cruces et al., 2019). 像这样, 这些
techniques could be used for the screening and subtyping of patients that may in turn become
candidates for targeted rehabilitative therapies. 此外, and beyond their increasingly
recognized utility in predicting seizure freedom postsurgery (Gleichgerrcht et al., 2020), 脑
network measures may potentially also help in the prognostication of post-operative outcomes
in cognitive and affective domains. A recent study has, 例如, shown an association
between resting-state fMRI degree centrality measures of the language network and postoper-
ative decline in naming in 20 patients undergoing left anterior temporal lobe resections
(Audrain et al., 2018), and a promising area of future research will thus investigate the asso-
ciation between pre- and postoperative network measures as well as pre- and postoperative
cognitive and affective markers.

Epilepsy is truly more than a seizure condition, and it is thus important to continue to iden-
tify underlying mechanisms of cognitive function across the spectrum of common epilepsies.
This expansion will involve increasing research efforts into less prevalent syndromes and

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further studying sources of interpatient variability. For these studies, we emphasize the need
to combine multidimensional cognitive phenotyping approaches with multimodal neuroim-
老化, given the likely complementary power of structural and functional imaging tech-
好的. As it is becoming increasingly evident from the current literature that cognitive
and affective dysfunction in the epilepsies likely relates to atypical neural organization at
different spatial and temporal scales, there will likely be an increased demand for advanced
analysis approaches. Such analyses include multivariate associative techniques, multilayer
network analysis, as well as machine learning approaches, and promise to address the likely
complex associations between brain network organization and dysfunction, while also
modeling effects of genetic, environmental, and disease factors. In TLE, prior clustering
and multivariate associative studies are already beginning to shed light on covariations in
atypical connectome organization and cognition, and further help to clarify sources of inter-
individual variations across the patient spectrum. Paralleling current trends in the study of
the brain and mental health, we recommend cross-syndrome investigations that can identify
shared and syndrome-specific effects on brain network organization and cognition. 这样的
approaches will provide higher granularity in studying the panorama of cognitive and affec-
tive impairments and associated connectome anomalies in TLE, ETE, and IGE. 最后, 到
generalize from potential idiosyncrasies of specific epilepsy centers and to allow for an unbi-
ased evaluation of network biomarkers in the prediction of dysfunction at the single-patient
等级, we recommend multisite data aggregation and analysis efforts such as ENIGMA-
Epilepsy (Sisodiya et al., 2020), along with strategies for prospective as well as retrospective
data harmonization at the level of brain and cognition alike.

CITATION DIVERSITY STATEMENT

Recent work in several fields of science has identified a bias in citation practices such that
papers from women and other minority scholars are undercited relative to the number of
such papers in the field (Dworkin et al., 2020; https://github.com/dalejn/cleanBib). 这里
we sought to proactively consider choosing references that reflect the diversity of the field
in thought, form of contribution, 性别, 种族, 种族, and other factors. 第一的, 我们得到了
the predicted gender of the first and last author of each reference by using databases that
store the probability of a first name being carried by a woman (Dworkin et al., 2020). By this
措施 (and excluding self-citations to the first and last authors of our current paper), 我们的
references contain 18.29% woman(第一的)/woman( 最后的), 9.4% man/woman, 23.16%
woman/man, 和 49.15% man/man. This method is limited in that (1) 名字, pronouns,
and social media profiles used to construct the databases may not, in every case, be indic-
ative of gender identity and (2) it cannot account for intersex, nonbinary, or transgender
人们. 第二, we obtained predicted racial/ethnic category of the first and last author
of each reference by databases that store the probability of a first and last name being car-
ried by an author of color (Sood & Laohaprapanon, 2018). By this measure (and excluding
self-citations), our references contain 13.13% author of color (第一的)/author of color (最后的),
11.24% white author/author of color, 25.8% author of color/white author, 和 49.84% 白色的
author/white author. This method is limited in that (1) names and Florida voter data to make
the predictions may not be indicative of racial/ethnic identity and (2) it cannot account for
Indigenous and mixed-race authors, or those who may face differential biases due to the
ambiguous racialization or ethnicization of their names. We look forward to future work that
could help us to better understand how to support equitable practices in science.

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Connectome biomarkers of cognitive/affective dysfunction in epilepsy

作者贡献

Raul Rodriguez-Cruces: 概念化; 调查; 可视化; 写作——原创
草稿; 写作——复习 & 编辑. Jessica Royer: 调查; 可视化; 写作——原创
草稿; 写作——复习 & 编辑. Sara Larivière: 写作——复习 & 编辑. Dani S. Bassett:
写作——复习 & 编辑. Lorenzo Caciagli: 概念化; Writing – original draft;
写作——复习 & 编辑. Boris C. Bernhardt: 概念化; 资金获取; Inves-
tigation; Writing – original draft; 写作——复习 & 编辑.

资金信息

Raul Rodriguez-Cruces, Fonds de la Recherche du Québec – Santé, 奖项ID: FRQ-S 291486.
Jessica Royer, Canadian Institute of Health Research, CIHR Fellowship. Boris C. Bernhardt,
National Science and Engineering Research Council of Canada, 奖项ID: NSERC
Discovery-1304413; Canadian Institute of Health Research, 奖项ID: FDN-154298;
Canadian Institute of Health Research, 奖项ID: PJT-174995; SickKids Foundation, 奖
ID: NI17-039; Azrieli Center for Autism Research (ACAR-TACC), New Investigator Research
授予; BrainCanada, Future Leaders Research Grant; Helmholtz International Bigbrain Analyt-
ics and Learning Laboratory (Hiball), FRQ-S, and the Tier-2 Canada Research Chairs program,
Tier-2. Sara Larivière, Canadian Institute of Health Research, CIHR doctoral award. Lorenzo
Caciagli and Dani S. Bassett, NINDS (R01-NS099348). Dani S. Bassett, John D. and Catherine
时间. 麦克阿瑟基金会; Alfred P. Sloan Foundation; the Paul Allen Family Foundation; 和
the ISI Foundation.

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