Peter Mariën1,2,  and Mario Manto3,4,     1Department of Neurology and Memory Clinic, ZNA General Hospital, Middelheim, Antwerp, Belgium;,     2Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium,     3Unité d’Etude du Mouvement, Université Libre de Bruxelles, Brussels, Belgium,     4Université de Mons, Mons, Belgium

In less than three decades, the concept of “cerebellar neurocognition” has evolved from a mere afterthought to an entirely new and multifaceted area of neuroscientific research. A close interplay among three main strands of contemporary neuroscience has induced a substantial modification of the traditional view of the cerebellum as a simple coordinator of autonomic and somatic motor functions. Indeed, the wealth of currently available evidence derived from (1) detailed neuroanatomical investigations, (2) functional neuroimaging studies with healthy subjects and patients, and (3) in-depth neuropsychological assessment of patients with cerebellar disorders shows that the cerebellum plays also a cardinal role in affective regulation, cognitive processing, and linguistic functions. However, although considerable progress has been made in models of cerebellar function, controversy remains regarding the exact role of the “linguistic cerebellum” in a broad variety of nonmotor language processes.

This volume brings together a range of different viewpoints and opinions regarding the contribution of the cerebellum to language function. Recent developments and insights in the nonmotor modulatory role of the cerebellum in language and some related disorders are discussed by experts in the field. The role of the cerebellum in speech and language perception, in motor speech planning including apraxia of speech, in verbal working memory, in phonological and semantic verbal fluency, in syntax processing, in the dynamics of language production, in reading, and in writing will be addressed. In addition, the functional topography of the linguistic cerebellum and the contribution of the deep nuclei to linguistic function will be discussed. As such, with this volume, we hope to offer a framework for debate and discussion. The reader interested in the neuroscientific mysteries of this organ situated at the bottom of the brain will find not only state-of-the-art contributions, but also novel ideas that are being investigated in a growing number of laboratories worldwide. The fact that the cerebellum contains more neurons than any other region of the brain and is characterized by a geometrical structure makes it an excellent candidate for investigation of novel concepts in neuroscience.

Two centuries of research on cerebellar function have been dominated by the role of the cerebellum in motor control (see Manto et al., 2012 for a review). However, from time to time, clinical case descriptions and experimental evidence from animal studies dating back to the early part of the nineteenth century, already suggested an association between cerebellar pathology and a variety of nonmotor cognitive as well as affective dysfunctions (see Schmahmann, 1991, 1997). As early as 1831, Combettes described in the Bulletins de la Société Anatomique de Paris, the postmortem findings of an 11-year-old girl, Alexandrine Labrosse, who presented with neurodevelopmental disorders including a range of cognitive, affective, and motor impairments resulting from a complete absence of the cerebellum (Figure 1).

Nevertheless, a causal connection between cerebellar disease and cognitive and affective disturbances was dismissed for decades. In the mid-1900s, investigators started to examine a possible link between the cerebellum and cognition and emotion, exemplified by the work of Snider and Eldred (1948), Snider (1950), Snider and Maiti (1976), Dow (1974), Heath (1977, 1997), Heath, Franklin, and Shraberg (1979), Cooper, Riklan, Amin, and Cullinan (1978) and others (see Schmahmann, 1991 for a review). This laid a foundation for the rediscovery of this concept by Leiner, Leiner, and Dow (1986, 1991), who hypothesized that more recently evolved parts of the cerebellum contribute to learning, cognition, and language, and by Schmahmann (1991) and Schmahmann and Pandya (1987, 1989), who introduced the dysmetria of thought hypothesis (Schmahmann, 1998). These authors provided a historical, clinical, neuroanatomical, and theoretical framework within which a cerebellar role in higher cognitive and affective processes could be considered. That there may be a correlation between the size of the cerebellum and aspects of general intelligence has been known for some time (e.g., Allin et al., 2001; Ciesielski, Harris, Hart, & Pabst, 1997; Mostofsky et al., 1998; Paradiso, Andreasen, O’Leary, Arndt, & Robinson, 1997). From an evolutionary perspective, MacLeod, Zilles, Schleicher, Rilling, and Gibson (2003) demonstrated a reliable linear regression contrast between volumes of whole brain, cerebellum, vermis, and hemisphere of hominoids and monkeys and a striking increase in the lateral cerebellum in hominoids (Beaton & Mariën, 2010). After controlling statistically for age and sex, Pangelinan et al. (2011) showed with school-aged children that total cerebellar volume correlates significantly with cognitive ability (as measured by overall intelligence quotient) (but see Parker et al. (2008) for negative findings). Posthuma et al. (2003) reported that cerebellar volume in healthy adults (as well as total cerebral grey and white matter volumes) correlates with working memory performance. Such findings make it difficult to deny that the cerebellum is “an organ of cognition” (Justus & Ivry, 2001).

Only a few years after the introduction of the dysmetria of thought theory, Schmahmann and Sherman (1998) 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” to describe this condition. Schmahmann syndrome, the eponym of cerebellar cognitive affective syndrome (Manto & Mariën, 2015), was characterized as a cluster of multimodal disturbances including: (1) executive deficits (deficient planning, set-shifting, abstract reasoning, working memory, and decreased verbal fluency), (2) disruption of visuospatial cognition (visuospatial disorganization and impaired visuospatial memory), (3) personality changes (flattening or blunting of affect, and disinhibited or inappropriate behavior), and (4) a range of linguistic impairments among which were dysprosodia, agrammatism, and mild anomia. However, analysis of the clinical data revealed that not all deficits occurred in each patient, but that certain symptoms were particularly prominent. Decreased verbal fluency, which did not relate to dysarthria, was said to be present in 18 of the 20 patients. Visuospatial disintegration, mainly consisting of disruption of the sequential approach to drawing and conceptualization of figures was found in 19 cases. Eighteen of the 20 patients presented with executive dysfunctions involving working memory, motor, and mental set-shifting and perseverations of actions and drawing. In 15 patients, frontal-like behavioral and affective changes were evident. Flattening of affect or disinhibition occurred, taking the form of overfamiliarity, flamboyant and impulsive actions, and humorous but inappropriate comments. Behavior was characterized as regressive and child-like in some cases and obsessive–compulsive traits were occasionally observed. Deficits in mental arithmetic were evident in 14 patients. Visual confrontation naming was impaired in 13 patients. Eight patients developed abnormal prosody characterized by high-pitched, whining, and a hypophonic speech quality. Mnestic deficits (verbal and visual learning and recall) were observed in some cases. The cluster of symptoms defining Schmahmann syndrome was associated with a decrease of general intellectual capacity. From an anatomoclinical perspective, cognitive and affective impairments were more prominent and generalized in patients with large, bilateral, or pancerebellar disorders, especially in a context of an acute onset of cerebellar disease. Posterior lobe damage was particularly important in the genesis of this novel syndrome. Damage of the vermal regions was consistently present in patients with disruption of affect. Anterior lobe damage was found to be less important to cause cognitive and behavioral deficits. Schmahmann syndrome in patients with stroke improved over time, but executive function remained abnormal. Schmahmann and Sherman (1998) pointed out that on the basis of their observations, it was not possible to distinguish the contribution of the lesioned cerebellum to these abnormal behaviors from that of the cerebral regions newly deprived of their connections with the cerebellum. Indeed, the clinical features of the cognitive and affective impairments constituting Schmahmann syndrome are identical to those usually identified in patients with supratentorial...