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Journal ArticleDOI

Consensus Paper: Cerebellum and Emotion

TL;DR: Results of this consensus paper illustrate how theory and empirical research have converged to produce a composite picture of brain topography, physiology, and function that establishes the role of the cerebellum in many aspects of emotional processing.
Abstract: Over the past three decades, insights into the role of the cerebellum in emotional processing have substantially increased. Indeed, methodological refinements in cerebellar lesion studies and major technological advancements in the field of neuroscience are in particular responsible to an exponential growth of knowledge on the topic. It is timely to review the available data and to critically evaluate the current status of the role of the cerebellum in emotion and related domains. The main aim of this article is to present an overview of current facts and ongoing debates relating to clinical, neuroimaging, and neurophysiological findings on the role of the cerebellum in key aspects of emotion. Experts in the field of cerebellar research discuss the range of cerebellar contributions to emotion in nine topics. Topics include the role of the cerebellum in perception and recognition, forwarding and encoding of emotional information, and the experience and regulation of emotional states in relation to motor, cognitive, and social behaviors. In addition, perspectives including cerebellar involvement in emotional learning, pain, emotional aspects of speech, and neuropsychiatric aspects of the cerebellum in mood disorders are briefly discussed. Results of this consensus paper illustrate how theory and empirical research have converged to produce a composite picture of brain topography, physiology, and function that establishes the role of the cerebellum in many aspects of emotional processing.

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City, University of London Institutional Repository
Citation: Adamaszek, M., D'Agata, F., Ferrucci, R., Habas, C., Keulen, S., Kirkby, K.C.,
Leggio, M., Marien, P., Molinari, M., Moulton, E., Orsi, L., Van Overwalle, F., Papadelis, C.,
Priori, A., Sacchetti, B., Schutter, D.J., Styliadis, C. and Verhoeven, J. (2017). Consensus
Paper: Cerebellum and Emotion. Cerebellum, 16(2), pp. 552-576. doi: 10.1007/s12311-016-
0815-8
This is the accepted version of the paper.
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version.
Permanent repository link: https://openaccess.city.ac.uk/id/eprint/16660/
Link to published version: http://dx.doi.org/10.1007/s12311-016-0815-8
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CONSENSUSPAPER: CEREBELLUM AND EMOTIONS
M. ADAMASZEK ET AL.
The cerebellum, language and emotion: the role of emotional prosody
Stefanie Keulen
1, 2
, Jo Verhoeven
3
, Frank Van Overwalle
4
, Peter Mariën
1, 5
1
Department of Clinical and Experimental Neurolinguistics, CLIEN, Vrije Universiteit
Brussel, Brussels, Belgium
2
Center for Language and Cognition Groningen, Rijksuniversiteit Groningen,
Groningen, The Netherlands
3
Department of Language and Communication Science, City University, London, UK
4
Faculty of Psychology and Educational Sciences, Vrije Universiteit Brussel, Brussels,
Belgium.
5
Department of Neurology and Memory Clinic, ZNA Middelheim General Hospital,
Antwerp, Belgium
During the past decades, the traditional view of the cerebellum as a mediator of motor
function has been thoroughly revised and it has been recognized that the cerebellum
subserves a wide range of neurocognitive, linguistic, affective and social functions (De
Smet et al., 2013; Schmahmann, 2004; Beaton and Mariën, 2010; Van Overwalle et al.,
2014).
A crucial aspect of speech is the role of prosody, i.e. the melody and rhythm of
speech which supports the meaning of linguistic units (e.g. words, phrases or sentences).
Prosody results from the complex interplay of several acoustic variables such as pitch,
loudness and rhythm (Sidtis and Van Lancker Sidtis, 2003) which are typically affected
after cerebellar pathology. In his hallmark 1917-paper Gordon Holmes described
impaired speech following cerebellar damage as typically slow, monotonous, staccato,
scanned, indistinct, remarkably irregular, jerky, explosive, slurred, and laboured
resulting in what was later called ataxic dysarthria and dysprosodia.
In the past, two main types of prosody have generally been distinguished:
linguistic (or propositional) and emotional (or affective) prosody. Linguistic prosody
supports the distinction between different sentence types by means of intonation (e.g.

interrogative and declarative sentences), but also between word categories by means of
word stress (e.g. /ˈædrɛs/ (noun) versus /əˈdrɛs/ (verb)). Emotional prosody modulates
content in such a way that it conveys information about the emotional state of the
speaker. In early models, the expression and comprehension of emotional prosody were
typically situated in the homologous, non-dominant areas for expression and
comprehension of language, i.e. the inferior frontal gyrus and the posterior temporal
gyrus of the non-dominant hemisphere (see also: Wildgruber et al., 2006; Ross, 1981;
Sidtis and Van Lancker Sidtis, 2003). However, recent studies have shown that both
types of prosody require bilateral cerebral and even subcortical involvement to some
degree (e.g. Le Jeune et al., 2008; Chancelliere and Kertesz, 1990; Van Lancker and
Sidtis, 1992; Kotz et al., 2003; Mitchell et al., 2003). The different prosodic modalities
have been associated with different neural correlates. Wildgruber et al. (2006), Dapretto
et al. (1999) (perception tasks) and Mayer et al. (2002) (production tasks) found that
linguistic prosody is selectively associated with activity in the language dominant
inferior frontal and superior temporal gyrus (STG). Dogil et al. (2002) (same experiment
as Mayer et al., 2002), found increased BOLD-response in the language dominant STG
(when modulating rendering pitch accents: ‘focus’), and in the posterior part of the non-
dominant STG extending into the middle temporal gyrus (when modulating tone
boundaryrendering boundary tones: ‘modus’). Emotional prosody perceptionThe
perception of emotional prosody was variably associated with non-dominant inferior
frontal gyrus activity (Dapretto et al., 1999), bilateral orbito-frontal activity (Wildgruber
et al., 2006) and activation in the anterior part of the non-dominant STG (‘affect’-mode
in Dogil et al., 2002). Dogil et al. (2002) concluded that ‘… exclusively neocortical areas
[are] critically involved in prosody generation’ (p. 78). Nonetheless, studies have shown
that subcortical lesions encompassing the putamen and globus pallidus induce mood
disorders with deficits in emotional prosodic production (Van Lancker Sidtis et al.,
2006). It has been argued that the source for dysprosody may lie in deficits of timingis
caused by a timing deficit (Sidtis and Van Lancker Sidtis, 2003), with timing being a
fundamental role of the cerebellum in motor execution processing.
Recent functional neuroimaging studies have confirmed a possible role for of the
cerebellum in the processing of emotional prosody. In an fMRI study of emotional
prosody comprehensionrecognition, in which participants listened to numbers
pronounced with prosodic manipulation inferring suggesting neutral versus simple

(happy, sad, angry) and complex (guilt, proud, bored) emotions, Alba-Ferrara et al.
(2011) found significantly increased metabolic activation in the right cerebellum
(Z=3.29) (in the presence of several left and right-hemisphere mostly frontal, including
(para)limbic activations). This activation was still also present when comparing
complex with and simple emotions (Z=3.62), even when controlled for pitch (Z=3.66).
Strelnikov et al. (2006) studied the perception of speech prosody in read sentences with
PET and apart from activity in the right dorsolateral prefrontal cortex (PFC), they also
observed activity in the right posterior lobe of the cerebellum. The area mediating
functional overlap between the differentially affected domains (prosody, syntax and
emotion) was the right posterior PFC. Right cerebellar activity was primarily related to
speech timing perception. According to Pichon and Kell (2013) the cerebellar vermis
modulates fundamental frequency in emotional speech production, as increased BOLD
response was evoked triggered in the cerebellum, thalamus, globus pallidus, substantia
nigra and superior temporal sulcus in especially the right hemisphere. Krienen et al.
(2009) argued the existence of segregated fronto-cerebellar circuits: one originating in
the medial PFC, which is connected to Crus I of the limbic cerebellum (Stoodley and
Schmahmann, 2009; Adamaszek et al., 2013; Alalade et al., 2011). Lesion studies and
studies in degenerative cerebellar disorders have provided additional evidence for the
involvement of the cerebellum in (disrupted) emotional prosody. Sokolovsky et al.
(2010) described impaired verbal emotion attribution in patients with spinocerebellar
ataxia whereas Adamaszek et al. (2013) reported difficulties in prosody naming and
prosody matching in a group of 15 patients with discrete ischemic cerebellar lesions.
They equally also found a correlation between volume of the lesion and the amount
number of errors in emotional and complex tasks.
Although a the role for of the cerebellum in emotional speech processing has not
been thoroughly investigated, the currently available evidence of cerebellar involvement
in the processing of emotional prosody as a marker of prosody timing is growing. Future
research will further unveil reveal the multifaceted role of the cerebellocerebral
circuitry in the linguistic production and perception of ‘emotions and affect’.
REFERENCES

Citations
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TL;DR: The ability to detect the CCAS in real time in clinical neurology with a brief and validated scale should make it possible to develop a deeper understanding of the clinical consequences of cerebellar lesions in a wide range of neurological and neuropsychiatric disorders with a link to the cerebellum.

1,002 citations

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TL;DR: Cerebellar task topography is described in the largest single cohort studied to date and three distinct representations each for working memory, language, social, and emotional task processing that were largely separate for these four cognitive and affective domains are revealed.

277 citations

Journal ArticleDOI
01 Jan 2018-Brain
TL;DR: A 10-item scale providing total raw score, cut-offs for each test, and pass/fail criteria that determined 'possible', 'probable', and 'definite' CCAS is derived, useful for expedited clinical assessment of CCAS in patients with cerebellar disorders.
Abstract: Cerebellar cognitive affective syndrome (CCAS; Schmahmann's syndrome) is characterized by deficits in executive function, linguistic processing, spatial cognition, and affect regulation. Diagnosis currently relies on detailed neuropsychological testing. The aim of this study was to develop an office or bedside cognitive screen to help identify CCAS in cerebellar patients. Secondary objectives were to evaluate whether available brief tests of mental function detect cognitive impairment in cerebellar patients, whether cognitive performance is different in patients with isolated cerebellar lesions versus complex cerebrocerebellar pathology, and whether there are cognitive deficits that should raise red flags about extra-cerebellar pathology. Comprehensive standard neuropsychological tests, experimental measures and clinical rating scales were administered to 77 patients with cerebellar disease-36 isolated cerebellar degeneration or injury, and 41 complex cerebrocerebellar pathology-and to healthy matched controls. Tests that differentiated patients from controls were used to develop a screening instrument that includes the cardinal elements of CCAS. We validated this new scale in a new cohort of 39 cerebellar patients and 55 healthy controls. We confirm the defining features of CCAS using neuropsychological measures. Deficits in executive function were most pronounced for working memory, mental flexibility, and abstract reasoning. Language deficits included verb for noun generation and phonemic > semantic fluency. Visual spatial function was degraded in performance and interpretation of visual stimuli. Neuropsychiatric features included impairments in attentional control, emotional control, psychosis spectrum disorders and social skill set. From these results, we derived a 10-item scale providing total raw score, cut-offs for each test, and pass/fail criteria that determined 'possible' (one test failed), 'probable' (two tests failed), and 'definite' CCAS (three tests failed). When applied to the exploratory cohort, and administered to the validation cohort, the CCAS/Schmahmann scale identified sensitivity and selectivity, respectively as possible exploratory cohort: 85%/74%, validation cohort: 95%/78%; probable exploratory cohort: 58%/94%, validation cohort: 82%/93%; and definite exploratory cohort: 48%/100%, validation cohort: 46%/100%. In patients in the exploratory cohort, Mini-Mental State Examination and Montreal Cognitive Assessment scores were within normal range. Complex cerebrocerebellar disease patients were impaired on similarities in comparison to isolated cerebellar disease. Inability to recall words from multiple choice occurred only in patients with extra-cerebellar disease. The CCAS/Schmahmann syndrome scale is useful for expedited clinical assessment of CCAS in patients with cerebellar disorders.awx317media15678692096001.

259 citations


Cites background from "Consensus Paper: Cerebellum and Emo..."

  • ...The defining features of CCAS have been replicated in studies across disease types and in patients of different ages (Malm et al., 1998; Levisohn et al., 2000; Neau et al., 2000; Riva and Giorgi, 2000; Exner et al., 2004; Paulus et al., 2004; Van Harskamp et al., 2005; Schmahmann et al., 2007; Caroppo et al., 2009; Mariën et al., 2009, 2014; Fallows et al., 2011; Tedesco et al., 2011; Wingeier et al., 2011; Hoche et al., 2014; Koziol et al., 2014; Van Overwalle et al., 2015; Adamaszek et al., 2017)....

    [...]

  • ...…et al., 2004; Paulus et al., 2004; Van Harskamp et al., 2005; Schmahmann et al., 2007; Caroppo et al., 2009; Mariën et al., 2009, 2014; Fallows et al., 2011; Tedesco et al., 2011; Wingeier et al., 2011; Hoche et al., 2014; Koziol et al., 2014; Van Overwalle et al., 2015; Adamaszek et al., 2017)....

    [...]

Journal ArticleDOI
TL;DR: The paper substantiates the concept of CCAS with recent evidence from different scientific angles, promotes awareness of the CCAS as a clinical entity, and examines the current insight into the therapeutic options available.
Abstract: Sporadically advocated over the last two centuries, a cerebellar role in cognition and affect has been rigorously established in the past few decades. In the clinical domain, such progress is epitomized by the “cerebellar cognitive affective syndrome” (“CCAS”) or “Schmahmann syndrome.” Introduced in the late 1990s, CCAS reflects a constellation of cerebellar-induced sequelae, comprising deficits in executive function, visuospatial cognition, emotion–affect, and language, over and above speech. The CCAS thus offers excellent grounds to investigate the functional topography of the cerebellum, and, ultimately, illustrate the precise mechanisms by which the cerebellum modulates cognition and affect. The primary objective of this task force paper is thus to stimulate further research in this area. After providing an up-to-date overview of the fundamental findings on cerebellar neurocognition, the paper substantiates the concept of CCAS with recent evidence from different scientific angles, promotes awareness of the CCAS as a clinical entity, and examines our current insight into the therapeutic options available. The paper finally identifies topics of divergence and outstanding questions for further research.

192 citations

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TL;DR: A comprehensive review of neuroimaging studies of suicidal thoughts and behaviors is presented in this paper, which summarizes the progress achieved on elucidating neurobiological substrates of STBs, with a focus on converging findings across studies.
Abstract: Identifying brain alterations that contribute to suicidal thoughts and behaviors (STBs) are important to develop more targeted and effective strategies to prevent suicide. In the last decade, and especially in the last 5 years, there has been exponential growth in the number of neuroimaging studies reporting structural and functional brain circuitry correlates of STBs. Within this narrative review, we conducted a comprehensive review of neuroimaging studies of STBs published to date and summarize the progress achieved on elucidating neurobiological substrates of STBs, with a focus on converging findings across studies. We review neuroimaging evidence across differing mental disorders for structural, functional, and molecular alterations in association with STBs, which converges particularly in regions of brain systems that subserve emotion and impulse regulation including the ventral prefrontal cortex (VPFC) and dorsal PFC (DPFC), insula and their mesial temporal, striatal and posterior connection sites, as well as in the connections between these brain areas. The reviewed literature suggests that impairments in medial and lateral VPFC regions and their connections may be important in the excessive negative and blunted positive internal states that can stimulate suicidal ideation, and that impairments in a DPFC and inferior frontal gyrus (IFG) system may be important in suicide attempt behaviors. A combination of VPFC and DPFC system disturbances may lead to very high risk circumstances in which suicidal ideation is converted to lethal actions via decreased top-down inhibition of behavior and/or maladaptive, inflexible decision-making and planning. The dorsal anterior cingulate cortex and insula may play important roles in switching between these VPFC and DPFC systems, which may contribute to the transition from suicide thoughts to behaviors. Future neuroimaging research of larger sample sizes, including global efforts, longitudinal designs, and careful consideration of developmental stages, and sex and gender, will facilitate more effectively targeted preventions and interventions to reduce loss of life to suicide.

184 citations

References
More filters
Journal ArticleDOI
TL;DR: Two distinct networks typically coactivated during functional MRI tasks are identified, anchored by dorsal anterior cingulate and orbital frontoinsular cortices with robust connectivity to subcortical and limbic structures, and an “executive-control network” that links dorsolateral frontal and parietal neocortices.
Abstract: Variations in neural circuitry, inherited or acquired, may underlie important individual differences in thought, feeling, and action patterns. Here, we used task-free connectivity analyses to isolate and characterize two distinct networks typically coactivated during functional MRI tasks. We identified a "salience network," anchored by dorsal anterior cingulate (dACC) and orbital frontoinsular cortices with robust connectivity to subcortical and limbic structures, and an "executive-control network" that links dorsolateral frontal and parietal neocortices. These intrinsic connectivity networks showed dissociable correlations with functions measured outside the scanner. Prescan anxiety ratings correlated with intrinsic functional connectivity of the dACC node of the salience network, but with no region in the executive-control network, whereas executive task performance correlated with lateral parietal nodes of the executive-control network, but with no region in the salience network. Our findings suggest that task-free analysis of intrinsic connectivity networks may help elucidate the neural architectures that support fundamental aspects of human behavior.

6,049 citations


"Consensus Paper: Cerebellum and Emo..." refers background in this paper

  • ...Resting-State Functional Connectivity An independent component analysis found at rest that the salience network involved in interoception, autonomic, and emotional regulation [103] encompasses vermal and hemispheric parts of the lobule VI as well as the adjacent Crus I and dentate nuclei [93]....

    [...]

01 Jan 1995
TL;DR: The International Affective Picture System (IAPS) as mentioned in this paper provides a set of normative emotional stimuli for experimental investigations of emotion and attention for the NIMH Center for Emotion and Attention.
Abstract: The International Affective Picture System (IAPS) is being developed to provide a set of normative emotional stimuli for experimental investigations of emotion and attention. The goal is to develop a large set of standardized, emotionally-evocative, internationally accessible, color photographs that includes contents across a wide range of semantic categories. The IAPS (pronounced EYE-APS), along with the International Affective Digitized Sound system (IADS), the Affective Lexicon of English Words (ANEW), as well as other collections of affective stimuli, are being developed and distributed by the NIMH Center for Emotion and Attention (CSEA) at the University of Florida in order to provide standardized materials that are available to researchers in the study of emotion and attention. The existence of these collections of normatively rated affective stimuli should: 1) allow better experimental control in the selection of emotional stimuli, 2) facilitate the comparison of results across different studies conducted in the same or different laboratory, and 3) encourage and allow exact replications within and across research labs who are assessing basic and applied problems in psychological science.

2,795 citations

Journal ArticleDOI
TL;DR: A systematic review of the literature regarding how activity in diverse brain regions creates and modulates the experience of acute and chronic pain states, emphasizing the contribution of various imaging techniques to emerging concepts is presented in this paper.

2,686 citations

Journal ArticleDOI
01 Apr 1998-Brain
TL;DR: A constellation of deficits is suggestive of disruption of the Cerebellar modulation of neural circuits that link prefrontal, posterior parietal, superior temporal and limbic cortices with the cerebellum, called the 'cerebellar cognitive affective syndrome'.
Abstract: Anatomical, physiological and functional neuroimaging studies suggest that the cerebellum participates in the organization of higher order function, but there are very few descriptions of clinically relevant cases that address this possibility. We performed neurological examinations, bedside mental state tests, neuropsychological studies and anatomical neuroimaging on 20 patients with diseases confined to the cerebellum, and evaluated the nature and severity of the changes in neurological and mental function. Behavioural changes were clinically prominent in patients with lesions involving the posterior lobe of the cerebellum and the vermis, and in some cases they were the most noticeable aspects of the presentation. These changes were characterized by: impairment of executive functions such as planning, set-shifting, verbal fluency, abstract reasoning and working memory; difficulties with spatial cognition including visual-spatial organization and memory; personality change with blunting of affect or disinhibited and inappropriate behaviour; and language deficits including agrammatism and dysprosodia. Lesions of the anterior lobe of the cerebellum produced only minor changes in executive and visual-spatial functions. We have called this newly defined clinical entity the 'cerebellar cognitive affective syndrome'. The constellation of deficits is suggestive of disruption of the cerebellar modulation of neural circuits that link prefrontal, posterior parietal, superior temporal and limbic cortices with the cerebellum.

2,640 citations


"Consensus Paper: Cerebellum and Emo..." refers background in this paper

  • ...However, several data support the view that a third well-delineated cerebellar limbic zone specifically devoted to emotional processing must be added [1, 94]....

    [...]

  • ..., cognition, affect, and motor function [1]), such as somatosensory cortices, periaqueductal gray, anterior cingulate cortex, dorsolateral prefrontal cortices, basal ganglia, hippocampus, hypothalamus, and amygdala [126–128]....

    [...]

  • ...Only a few years after the introduction of the dysmetria of thought theory, Schmahmann and Sherman [1] described in a seminal study of patients with focal cerebellar lesions a consistent pattern of cognitive and affective deficits and coined the term “cerebellar cognitive affective syndrome” (CCAS) to describe this condition....

    [...]

  • ...Schmahmann, Weilburg, and Sherman [20] grouped the wide range of cerebellar behavioral and emotional disorders in five major categories—attentional control, emotional control, autism spectrum, psychosis spectrum, and social skill set....

    [...]

Journal ArticleDOI
TL;DR: An activation likelihood estimate (ALE) meta-analysis of neuroimaging studies reporting cerebellar activation in selected task categories provided support for an anterior sensorimotor vs. posterior cognitive/emotional dichotomy in the human cerebellum.

1,730 citations


"Consensus Paper: Cerebellum and Emo..." refers background in this paper

  • ...Meta-analyses found emotion-related activity in vermal lobule VIIAt [7], left Crus I and right lobule VI [7, 101], right lobules...

    [...]

  • ...Neuroimaging of Emotional Processing in the Cerebellum Neuroimaging studies indicate that negative emotions correlate with activity in left VI, right IV/V, and bilateral Crus I and positive emotions with right VI activity [7, 133]....

    [...]

  • ...Of note are the medial cerebellum, in particular the vermis, and lobules VI and Crus I in the lateral cerebellum, and their reciprocal connections to the prefrontal cortex and temporal lobes [7]....

    [...]

  • ...key region among the emotion relevant structures [7, 8], and distinct subregions of the cerebellum are selectively involved in different primary emotions [9]....

    [...]

  • ...[160] argued the existence of segregated fronto-cerebellar circuits: one originating in the medial PFC, which is connected to Crus I of the limbic cerebellum [7, 43, 161]....

    [...]

Frequently Asked Questions (6)
Q1. What is the role of the cerebellum in the processing of emotional speech?

According to Pichon and Kell (2013) the cerebellar vermis modulates fundamental frequency in emotional speech production, as increased BOLD response was evoked triggered in the cerebellum, thalamus, globus pallidus, substantia nigra and superior temporal sulcus in especially the right hemisphere. 

Prosody results from the complex interplay of several acoustic variables such as pitch, loudness and rhythm (Sidtis and Van Lancker Sidtis, 2003) which are typically affected after cerebellar pathology. 

The area mediating functional overlap between the differentially affected domains (prosody, syntax and emotion) was the right posterior PFC. 

In an fMRI study of emotional prosody comprehensionrecognition, in which participants listened to numbers pronounced with prosodic manipulation inferring suggesting neutral versus simple(happy, sad, angry) and complex (guilt, proud, bored) emotions, Alba-Ferrara et al. (2011) found significantly increased metabolic activation in the right cerebellum (Z=3.29) (in the presence of several left and right-hemisphere – mostly frontal, including (para)limbic – activations). 

studies have shown that subcortical lesions encompassing the putamen and globus pallidus induce mood disorders with deficits in emotional prosodic production (Van Lancker Sidtis et al., 2006). 

5 Department of Neurology and Memory Clinic, ZNA Middelheim General Hospital,Antwerp, BelgiumDuring the past decades, the traditional view of the cerebellum as a mediator of motor function has been thoroughly revised and it has been recognized that the cerebellum subserves a wide range of neurocognitive, linguistic, affective and social functions (De Smet et al., 2013; Schmahmann, 2004; Beaton and Mariën, 2010; Van Overwalle et al., 2014).