Brain & Language 127 (2013) 315–316
Contents lists available at ScienceDirect
Brain & Language journal homepage: www.elsevier.com/locate/b&l
Editorial
The contribution of the cerebellum to speech and language
By and large, the systematic experimental analysis of cerebellar functions traces back to Luigi Rolando who conducted ablation studies in a variety of species around the turn of the 18th to 19th century (Schmahmann, 2010). He found damage to the cerebellum to compromise motor activities of the homolateral body side, but to spare the – in more recent parlance – sensory, autonomic and cognitive domains. Holmes (1917, 1939) provided the classical description of cerebellar movement abnormalities in humans. Besides, e.g., unsteady postural equilibrium and staggering gait, he observed ‘‘distinct disorders of voluntary movement’’ referred to, usually, as ‘‘ataxia’’ or ‘‘incoordination’’. Again, cerebellar symptomatology was found restricted, by and large, to the motor domain – a teaching passed down over generations of neurological textbooks until about two decades ago. The ‘‘distinct disorders of voluntary movement’’ in cerebellar disorders may affect speech motor control a well. Holmes (1917) provided the first more detailed account of these abnormalities of spoken language. His early observations are, more or less, in line with the still authoritative auditory-perceptual investigation of the Mayo Clinic, based upon patients with different etiological variants of a cerebellar syndrome (see Duffy, 2005 for a recent review). Imprecise consonants and distorted vowels, irregular articulatory breakdown, ‘‘excess and equal stress’’, i.e., scanning speech rhythm, reduced speaking rate as well as harsh voice quality emerged as the most salient features – a profile of speech motor deficits called ‘‘ataxic dysarthria’’. However, it remains unclear in how far extra-cerebellar pathology contributed to the data – given the rather limited diagnostic opportunities available at that time. More recent studies tried to recruit patients with a disease process restricted to the cerebellum as documented by neuroradiological techniques (see the contribution of Urban this volume) or subjects with a molecular-genetic diagnosis of a distinct hereditary degenerative disease entity affecting predominantly a specific subcomponent of the cerebellum (Schalling & Hartelius this volume). These data should allow for a more precise ‘‘localization’’ of ataxic dysarthria within the cerebellum and could provide a more refined specification of the contribution of the cerebellum proper to speech production. The overall volume of the cerebellum varies considerably across vertebrate classes - even after scaling to body or hindbrain size. Furthermore, the various macroscopic components of this organ may show a differential enlargement across species – related, allegedly, to specific behavioral traits such as beak control in woodpeckers (Sultan & Glickstein, 2007). Most noteworthy, structural magnetic resonance imaging (MRI) points at a conjoint relative enlargement of the cerebellar lobules connected with prefrontal areas in our species (Balsters et al., 2010), suggesting an engagement of the cerebellum in cognitive functions and skills. As more direct evidence, systematic neuropsychological studies in 0093-934X/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.bandl.2013.10.006
larger group of patients with pathology restricted to the cerebellum revealed – beyond the preceding rather anecdotal clinical observations – compromised executive functions (verbal working memory, set-shifting, etc.), impaired visual-spatial capacities, memory deficits, and personality changes (Schmahmann & Sherman, 1998). In accordance with these clinical data, imaging studies point, indeed, at a functional compartmentalization of the cerebellar cortex in that motor, cognitive and ‘‘limbic’’ tasks elicit activation patterns of a distinct topographical distribution each (Schmahmann, 2010). In addition, a variety of higher-order abnormalities of spoken language – more or less exclusive agrammatism as well as amnesic or transcortical motor aphasia – have been noted – although rather sporadically – in patients with cerebellar vascular lesions (De Smet et al. this volume) and – more frequently – during the course of recovery from a syndrome of transient mutism following resection of posterior fossa tumors, especially, in children (Küper & Timmann this volume). Neuroradiological investigations point at ‘‘crossed cerebello-cerebral diaschisis’’ as a potential pathomechanism both of cerebellar agrammatism/aphasia and cerebellar mutism, i.e., ‘‘functional depression’’ of frontal areas reciprocally interconnected with the damaged cerebellar region – translating into reduced blood flow (hypoperfusion) and decreased oxygen consumption of the affected supratentorial structures. As a consequence, these constellations must not be considered a cerebellar dysfunction proper, but a disorder of frontal cortex. In a phylogenetic perspective, inner speech mechanisms – based on a pre-articulatory verbal code – may have ‘‘emerged from overt speech and motor systems as an evolutionary adaptive way to boost cognitive processes that rely on working memory, such as languge acquisition’’ (Marvel & Desmond, 2010, p. 8). Conceivably, the computational power of the cerebellum also subserves the temporal organization of the sound structure of utterances at a pre-articulatory level in terms, e.g., of the adjustment of syllable lengths, including the ‘‘speaking rate’’ of an internal verbal code (Ackermann, 2008). As a further argument in these regards, the cerebellum engages in the precise representation of temporal information in speech and non-speech perceptual tasks (e.g., Ivry & Fiez, 2000). Thus, cerebellar disorders may compromise cognitive operations dependent upon inner speech such as the subvocal rehearsal component of verbal working memory or may impede the linguistic scaffolding of executive functions. Tight reciprocal interactions – such as those between prefrontal cortex and the lateral cerebellar hemispheres during, e.g., verbal-executive tasks – represent a prerequisite for the emergence of crossed cerebello-cerebral diaschisis effects. An encroachment of frontal hypoperfusion upon Broca’s area or mesiofrontal premotor cortex could explain the - though rare - occurrence of transient higher-order linguistic deficits of spoken language in adults or the – more
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Editorial / Brain & Language 127 (2013) 315–316
frequent – emergence of transient mutism in children after acute damage to the cerebellum. References Ackermann, H. (2008). Cerebellar contributions to speech production and speech perception: Psycholinguistic and neurobiological perspectives. Trends in Neuroscience, 31, 265–272. Balsters, J. H., Cussans, E., Diedrichsen, J., Phillips, K. A., Preuss, T. M., Rilling, J. K., et al (2010). Evolution of the cerebellar cortex: The selective expansion of prefrontal-projecting cerebellar lobules. Neuroimage, 49, 2045–2052. Duffy, J. R. (2005). Motor speech disorders: Substrates, differential diagnosis, and management (2nd ed.). St. Louis, MO: Elsevier Mosby. Holmes, G. (1917). The symptoms of acute cerebellar injuries due to gunshot injuries. Brain, 40, 461–535. Holmes, G. (1939). The cerebellum of man. Brain, 62, 1–30. Ivry, R. B., & Fiez, J. A. (2000). Cerebellar contributions to cognition and imagery. In M. S. Gazzaniga (Ed.), The new cognitive neurosciences (2nd ed., pp. 999–1011). Cambridge, MA: MIT Press. Marvel, C. L., & Desmond, J. E. (2010). Functional topography of the cerebellum in verbal working memory. Neuropsychology Review, 20, 271–279.
Schmahmann, J. D. (2010). The role of the cerebellum in cognition and emotion: Personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychology Review, 20, 236–260. Schmahmann, J. D., & Sherman, J. C. (1998). The cerebellar cognitive affective syndrome. Brain, 121, 561–579. Sultan, F., & Glickstein, M. (2007). The cerebellum: Comparative and animal studies. Cerebellum, 6, 168–176.
Guest Editor Hermann Ackermann Department of General Neurology/Center for Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Hoppe-Seyler-Strasse 3, D-72076 Tübingen, Germany E-mail address: [email protected]
Contents lists available at ScienceDirect
Brain & Language journal homepage: www.elsevier.com/locate/b&l
Editorial
The contribution of the cerebellum to speech and language
By and large, the systematic experimental analysis of cerebellar functions traces back to Luigi Rolando who conducted ablation studies in a variety of species around the turn of the 18th to 19th century (Schmahmann, 2010). He found damage to the cerebellum to compromise motor activities of the homolateral body side, but to spare the – in more recent parlance – sensory, autonomic and cognitive domains. Holmes (1917, 1939) provided the classical description of cerebellar movement abnormalities in humans. Besides, e.g., unsteady postural equilibrium and staggering gait, he observed ‘‘distinct disorders of voluntary movement’’ referred to, usually, as ‘‘ataxia’’ or ‘‘incoordination’’. Again, cerebellar symptomatology was found restricted, by and large, to the motor domain – a teaching passed down over generations of neurological textbooks until about two decades ago. The ‘‘distinct disorders of voluntary movement’’ in cerebellar disorders may affect speech motor control a well. Holmes (1917) provided the first more detailed account of these abnormalities of spoken language. His early observations are, more or less, in line with the still authoritative auditory-perceptual investigation of the Mayo Clinic, based upon patients with different etiological variants of a cerebellar syndrome (see Duffy, 2005 for a recent review). Imprecise consonants and distorted vowels, irregular articulatory breakdown, ‘‘excess and equal stress’’, i.e., scanning speech rhythm, reduced speaking rate as well as harsh voice quality emerged as the most salient features – a profile of speech motor deficits called ‘‘ataxic dysarthria’’. However, it remains unclear in how far extra-cerebellar pathology contributed to the data – given the rather limited diagnostic opportunities available at that time. More recent studies tried to recruit patients with a disease process restricted to the cerebellum as documented by neuroradiological techniques (see the contribution of Urban this volume) or subjects with a molecular-genetic diagnosis of a distinct hereditary degenerative disease entity affecting predominantly a specific subcomponent of the cerebellum (Schalling & Hartelius this volume). These data should allow for a more precise ‘‘localization’’ of ataxic dysarthria within the cerebellum and could provide a more refined specification of the contribution of the cerebellum proper to speech production. The overall volume of the cerebellum varies considerably across vertebrate classes - even after scaling to body or hindbrain size. Furthermore, the various macroscopic components of this organ may show a differential enlargement across species – related, allegedly, to specific behavioral traits such as beak control in woodpeckers (Sultan & Glickstein, 2007). Most noteworthy, structural magnetic resonance imaging (MRI) points at a conjoint relative enlargement of the cerebellar lobules connected with prefrontal areas in our species (Balsters et al., 2010), suggesting an engagement of the cerebellum in cognitive functions and skills. As more direct evidence, systematic neuropsychological studies in 0093-934X/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.bandl.2013.10.006
larger group of patients with pathology restricted to the cerebellum revealed – beyond the preceding rather anecdotal clinical observations – compromised executive functions (verbal working memory, set-shifting, etc.), impaired visual-spatial capacities, memory deficits, and personality changes (Schmahmann & Sherman, 1998). In accordance with these clinical data, imaging studies point, indeed, at a functional compartmentalization of the cerebellar cortex in that motor, cognitive and ‘‘limbic’’ tasks elicit activation patterns of a distinct topographical distribution each (Schmahmann, 2010). In addition, a variety of higher-order abnormalities of spoken language – more or less exclusive agrammatism as well as amnesic or transcortical motor aphasia – have been noted – although rather sporadically – in patients with cerebellar vascular lesions (De Smet et al. this volume) and – more frequently – during the course of recovery from a syndrome of transient mutism following resection of posterior fossa tumors, especially, in children (Küper & Timmann this volume). Neuroradiological investigations point at ‘‘crossed cerebello-cerebral diaschisis’’ as a potential pathomechanism both of cerebellar agrammatism/aphasia and cerebellar mutism, i.e., ‘‘functional depression’’ of frontal areas reciprocally interconnected with the damaged cerebellar region – translating into reduced blood flow (hypoperfusion) and decreased oxygen consumption of the affected supratentorial structures. As a consequence, these constellations must not be considered a cerebellar dysfunction proper, but a disorder of frontal cortex. In a phylogenetic perspective, inner speech mechanisms – based on a pre-articulatory verbal code – may have ‘‘emerged from overt speech and motor systems as an evolutionary adaptive way to boost cognitive processes that rely on working memory, such as languge acquisition’’ (Marvel & Desmond, 2010, p. 8). Conceivably, the computational power of the cerebellum also subserves the temporal organization of the sound structure of utterances at a pre-articulatory level in terms, e.g., of the adjustment of syllable lengths, including the ‘‘speaking rate’’ of an internal verbal code (Ackermann, 2008). As a further argument in these regards, the cerebellum engages in the precise representation of temporal information in speech and non-speech perceptual tasks (e.g., Ivry & Fiez, 2000). Thus, cerebellar disorders may compromise cognitive operations dependent upon inner speech such as the subvocal rehearsal component of verbal working memory or may impede the linguistic scaffolding of executive functions. Tight reciprocal interactions – such as those between prefrontal cortex and the lateral cerebellar hemispheres during, e.g., verbal-executive tasks – represent a prerequisite for the emergence of crossed cerebello-cerebral diaschisis effects. An encroachment of frontal hypoperfusion upon Broca’s area or mesiofrontal premotor cortex could explain the - though rare - occurrence of transient higher-order linguistic deficits of spoken language in adults or the – more
316
Editorial / Brain & Language 127 (2013) 315–316
frequent – emergence of transient mutism in children after acute damage to the cerebellum. References Ackermann, H. (2008). Cerebellar contributions to speech production and speech perception: Psycholinguistic and neurobiological perspectives. Trends in Neuroscience, 31, 265–272. Balsters, J. H., Cussans, E., Diedrichsen, J., Phillips, K. A., Preuss, T. M., Rilling, J. K., et al (2010). Evolution of the cerebellar cortex: The selective expansion of prefrontal-projecting cerebellar lobules. Neuroimage, 49, 2045–2052. Duffy, J. R. (2005). Motor speech disorders: Substrates, differential diagnosis, and management (2nd ed.). St. Louis, MO: Elsevier Mosby. Holmes, G. (1917). The symptoms of acute cerebellar injuries due to gunshot injuries. Brain, 40, 461–535. Holmes, G. (1939). The cerebellum of man. Brain, 62, 1–30. Ivry, R. B., & Fiez, J. A. (2000). Cerebellar contributions to cognition and imagery. In M. S. Gazzaniga (Ed.), The new cognitive neurosciences (2nd ed., pp. 999–1011). Cambridge, MA: MIT Press. Marvel, C. L., & Desmond, J. E. (2010). Functional topography of the cerebellum in verbal working memory. Neuropsychology Review, 20, 271–279.
Schmahmann, J. D. (2010). The role of the cerebellum in cognition and emotion: Personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychology Review, 20, 236–260. Schmahmann, J. D., & Sherman, J. C. (1998). The cerebellar cognitive affective syndrome. Brain, 121, 561–579. Sultan, F., & Glickstein, M. (2007). The cerebellum: Comparative and animal studies. Cerebellum, 6, 168–176.
Guest Editor Hermann Ackermann Department of General Neurology/Center for Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Hoppe-Seyler-Strasse 3, D-72076 Tübingen, Germany E-mail address: [email protected]
