Embodied cognition and the cerebellum: Perspectives from the Dysmetria of Thought and the Universal Cerebellar Transform theories

Abstract

In this report, we analyze the relationship between embodied cognition and current theories of the cerebellum, particularly the Dysmetria of Thought theory and the concept of the Universal Cerebellar Transform (UCT). First, we describe the UCT and the Dysmetria of Thought theories, highlight evidence supporting these hypotheses and discuss their mechanisms, functions and relevance. We then propose the following relationships. (i) The UCT strengthens embodied cognition because it provides an example of embodiment where the nature and intensity of the dependence between cognitive, affective and sensorimotor processes are defined. (ii) Conversely, embodied cognition bolsters the UCT theory because it contextualizes a cerebellum-focused theory within a general neurological theory. (iii) Embodied cognition supports the extension to other brain regions of the principles of organization of cerebral cortical connections that underlie the UCT: The notion that cytoarchitectonically determined transforms manifest via connectivity as sensorimotor, cognitive and affective functions resonates with the embodiment thesis that cognitive, affective and sensorimotor systems are interdependent. (iv) Embodied cognition might shape future definitions of the UCT because embodiment redefines the relationship between the neurological systems modulated by the UCT. We conclude by analyzing the relationship between our hypotheses and the concept of syntax and action semantics deficits in motor diseases.

Introduction

The embodied cognition research program (Shapiro, 2007, Shapiro, 2011) (hereafter, embodied cognition) reconfigures the nature of cognition by regarding the body and the environment as significant factors in the way we think and feel. This line of inquiry explores the extent to which “aspects of the agent's body beyond the brain play a significant causal or physically constitutive role in cognitive processing” (Wilson & Foglia, 2016). It includes the study of the relationship between sensorimotor, cognitive and affective neurological systems. The notion of embodied cognition emerged from a wide diversity of empirical observations and theoretical reflections, from Heidegger's analysis of being-in-the-world (Heidegger, 1962) to behavioral and functional neuroimaging experiments (e.g., Hauk, Johnsrude, & Pulvermüller, 2004). In the present analysis, we develop the hypothesis that there is a strong mutual interaction between the fields of embodied cognition and the cognitive neuroscience of the cerebellum. Specifically, we focus on the relationship between sensorimotor, cognitive and affective neurological systems inherent in embodied cognition (see Wilson, 2002; “Off-Line Cognition Is Body Based”) and two fundamental theoretical underpinnings of cerebellar cognition – Dysmetria of Thought and the Universal Cerebellar Transform (UCT).

Studies exploring the role of sensorimotor systems in cognition and emotion support the notion that action cognition is grounded in the sensorimotor system. Understanding sensorimotor concepts activates sensorimotor cortices (Hauk et al., 2004, Tettamanti et al., 2005); listening to action sentences related to the hand or foot results in slower response times and decreased amplitude of motor evoked potentials recorded from the muscles of the hand and foot (Buccino et al., 2005); and lesions of sensorimotor cortices impair action-related linguistic abilities (Kemmerer, Rudrauf, Manzel, & Tranel, 2012). The formation of abstract concepts unrelated to action cognition seems also to be influenced by sensorimotor processes. Squeezing a hard ball increases the chance of judging sex-ambiguous faces as male (Slepian, Weisbuch, Rule, & Ambady, 2011); hand sanitizer was preferred after lying in an e-mail (Lee & Schwarz, 2010); holding hot coffee makes it more likely that one will judge a person as having a warmer personality and holding a hot therapeutic pad increases the likelihood of choosing a gift for a friend instead of for oneself (Williams & Bargh, 2008); and individuals judge an issue as more important when holding a heavy clipboard (Jostmann, Lakens, & Schubert, 2009; see, however, an ongoing discussion regarding the replicability of some of these findings [Rabelo, Keller, Pilati, & Wicherts, 2015], but also other studies reporting the influence of similar bodily sensations on a variety of abstract judgments [e.g., Schneider et al., 2015, Chandler et al., 2012, Ackerman et al., 2010]). Even everyday use of language seems to reflect a close relationship between sensorimotor principles and cognitive schemas. This is exemplified by statements such as “I have control over him”, or “He is under my control”, as argued in Lakoff's “Metaphors we live by” (Lakoff & Johnson, 1980).

Anatomical, clinical and neuroimaging findings suggest that the cerebellum is engaged not only in motor control but also in cognitive and affective functions (Baillieux et al., 2008, E et al., 2014, Middleton and Strick, 1994, Schmahmann and Pandya, 1989, Schmahmann, 1991, Schmahmann, 1996, Schmahmann and Sherman, 1998, Stoodley and Schmahmann, 2009, Stoodley et al., 2012; see also; Koziol et al., 2014, Ramnani, 2006, Schmahmann, 1997, Schmahmann, 2004, Sokolov et al., 2017). Although it has been argued that there are only minor connections between the cerebellum and cognitive areas of the cerebral cortex, that imaging evidence may be confounded by eye movements, and that cognitive deficits in cerebellar patients may result from damage to other brain structures (Glickstein, 1993, Glickstein and Doron, 2008), the sizeable body of evidence favors a role of the cerebellum in cognition and affect. In this way, the central question in cerebellar neurobiology is no longer whether the cerebellum plays a role in cognition and emotion, but instead how the cerebellum participates in these neurological functions. Recent publications highlight that “the functional participation of cerebellar structures in nonmotor cortical networks remains poorly understood and is highly understudied, despite the fact that the cerebellum possesses many more neurons than the cerebral cortex” (Brissenden, Levin, Osher, Halko, & Somers, 2016).

The theory of the UCT holds that the same neurological process subserves cerebellar modulation of movement, cognition and emotion. The Dysmetria of Thought theory, predicated on the notion of a UCT, posits that motor, cognitive and affective symptoms in cerebellar patients (the Cerebellar Cognitive Affective Syndrome [CCAS; Levisohn et al., 2000, Schmahmann and Sherman, 1998] or Schmahmann's syndrome [Manto & Mariën, 2015]) are consequences of a singular neurological dysfunction, the Universal Cerebellar Impairment. This manifests in the motor domain as dysmetria of movement (Holmes, 1939), and in the cognitive/affective domains as Dysmetria of Thought (Schmahmann, 1991, Schmahmann, 2000, Schmahmann, 2010) (Fig. 1).

The study of the UCT can be parsed into the following lines of analysis: (a) Does it exist? (b) What is its underlying mechanism or computation? (c) What is its function?

The existence of a UCT has been supported by the following observations:

• Cerebellar cortex cytoarchitecture is essentially constant throughout its structure (Ito, 1993, Voodg and Glickstein, 1998) – as function follows form, this uniform cerebellar anatomy suggests a uniform cerebellar function (Ito, 1993, Ramnani, 2006, Schmahmann, 1991, Schmahmann, 2001). A recent review (Cerminara, Lang, Sillitoe, & Apps, 2015) highlighted cerebellar anatomical, physiological, and genetic regional differences which have long been known to exist and argued that, in consequence, “the concept of a universal cerebellar transform probably does not hold true”. Indeed, cerebellar cortex cytoarchitecture is not completely uniform. The UCT theory has been developed on the observation of an essentially (yet not completely) uniform cerebellar cortical structure, contrasting with the heterogeneous cerebral cortical cytoarchitecture (Schmahmann, 2000: “Whereas immunohistochemistry has identified that cerebellar cortex contains anatomically identifiable parasagittal bands that appear to have connectional and physiologic specificity, there are no “Brodmann areas” in the cerebellum…The histology suggests that the transformations performed by the cerebellum are invariant throughout the structure.”). Other authors have argued similarly, e.g., “although there is some variation across the cortex, this is minor in relation to the scale of uniformity” (Ramnani, 2006).

• Cognitive and affective problems follow the logic of motor symptoms in patients with cerebellar injury – this common pattern of deficits is expected after the disruption of a common neurological process. Cerebellar damage impairs the rate, rhythm and accuracy of limb trajectories, but motor strength and power remain preserved. Similarly, damage to the cerebellum disrupts metalinguistic abilities, e.g., the ability to understand metaphorical expressions or to construct sentences with pragmatic quality, more than the basic structures of grammar and semantics. We showed this pattern of language deficits (Guell, Hoche, & Schmahmann, 2015) in a study in which the Oral Sentence Production Test, a constrained language task that examines basic semantic and syntactic abilities (Caplan & Hanna, 1998), revealed no deficits in patients with cerebellar injury. In contrast, the same patients had impaired performance on the Test of Language Competence – Expanded (Wiig & Secord, 1989), a test that examines metalinguistic abilities including the ability to identify alternative meanings of lexical and structural ambiguities, make logical inferences in short paragraphs, construct sentences with correct grammatical and pragmatic quality for a given context, and understand metaphorical expressions. Whereas cerebral cortical damage may result in loss of a function such as aphasia and paralysis, cerebellar damage degrades the precision, efficiency or coordination of that function as manifested in metalinguistic deficits or motor ataxia. Similarly, impairment in judging facial emotional expressions in cerebellar patients is understood as a deficit in a rapid, automatic and implicit processing of facial expressions (Hoche, Guell, Sherman, Vangel, & Schmahmann, 2016); and neuropsychiatric manifestations in cerebellar patients are conceptualized as an impairment in the implicit, automatic modulation of emotions (Schmahmann, Weilburg, & Sherman, 2007).

• Theta burst stimulation to two different cerebellar regions results in similar increases in the complexity and variability of brain signals across multiple time scales, i.e., multiscale entropy, in two different cerebral cortical regions (Farzan, Pascual-leone, Schmahmann, & Halko, 2016). This common pattern of electrophysiological changes is expected after the stimulation of a common neurological process.

• A precise connectivity map observed in tract tracing (see Schmahmann and Pandya, 1997, Schmahmann and Pandya, 2008; for a review; Dum & Strick, 2003), resting-state functional connectivity (Buckner et al., 2011, Habas et al., 2009, O'Reilly et al., 2010), and tractography studies (Granziera et al., 2009) links the cerebellum with multiple distinct sensorimotor, association and paralimbic areas of the cerebrum and allows a topographically specific cerebellar modulation of cerebral activity (Halko, Farzan, Eldaief, Schmahmann, & Pascual-leone, 2014). The notion of a singular neurological computation in the cerebellum might appear at odds with the remarkable diversity of cerebellar functions from movement coordination to cognition and emotion, and the presence of multiple distinct functional cerebellar subregions (E et al., 2014, Stoodley and Schmahmann, 2009, Stoodley et al., 2012). This apparent paradox is solved, however, by recognition of the connectional specificity of the cerebrocerebellar pathways which explains how functional topography and behavioral heterogeneity can emerge from a constant neurological process, the UCT.

Here we consider “function” to be the neurobehavioral outcome/consequence of a neural mechanism. In this view, a function may be inferred from behavioral observations. In contrast, we will consider “mechanism” to be the process by which a node in a distributed neural circuit performs its computation/transform necessary for the integrity of the network as a whole. Therefore, a mechanism may be ascertained from observations at multiple levels, including cellular physiology, neuroimaging, computational models, neuropsychological assessments, and clinical observations.

The original description of the concept of the UCT hypothesizes that the cerebellum performs its functions by acting as an oscillation dampener, rapidly and automatically optimizing performance according to context (Schmahmann, 1996). The definition is derived from the motor system and by analogy applies equally to the modulation of intellect and emotional processing. It is supported by behavioral observations: impairment in judging facial emotional expressions in cerebellar patients is understood as deficits in rapid, automatic and implicit processing of facial expressions (Hoche et al., 2016); metalinguistic deficits in cerebellar patients are conceptualized as disruptions in automatic adjustment of grammatical and semantic abilities to a linguistic context (Guell et al., 2015); and neuropsychiatric manifestations in cerebellar patients are viewed as an exaggeration (overshoot) or diminution (undershoot) of responses to the internal or external environment and as impairment in the implicit, automatic modulation of emotions (Schmahmann et al., 2007).

Additional investigations addressing the putative mechanisms underlying cerebellar functions have generated multiple (not mutually exclusive) hypotheses applicable to both motor and nonmotor domains, and these are compatible with the original concept of the UCT. These hypotheses include prediction (Miall et al., 2007, Lesage et al., 2012), event-timing (Ivry and Keele, 1989, Ivry et al., 2002), error-driven adjustment (Ben-Yehudah, Guediche, & Fiez, 2007), sequencing (Molinari, Chiricozzi, Clausi, & Tedesco, 2008), control of temporal dynamics (Farzan et al., 2016), and generation of internal models (Balsters and Ramnani, 2011, Ito, 2008). The latter holds that the cerebellum generates, and updates according to error-driven adjustment, internal models that mimic and predict motor and nonmotor behavior. These models influence the cerebral control of motor and nonmotor behavior (forward model), or directly manipulate the final outputs of sensorimotor, cognitive and affective functions (inverse models) (see Ito, 2008, Ishikawa et al., 2016, Ramnani, 2006 for a discussion on forward vs inverse models and their supporting evidence). The internal models hypothesis largely overlaps with studies supporting a role of the cerebellum in prediction, timing, sequencing, and error-driven adjustment (as reviewed in Sokolov et al., 2017). These hypotheses are derived from observations at multiple levels, including cellular physiology, cytoarchitecture and cerebrocerebellar interactions (e.g., Ito, 2008, Schmahmann, 1996), neuroimaging (e.g., Balsters & Ramnani, 2011), computational models (e.g., Wolpert, Miall, & Kawato, 1998), electroencephalography and theta burst transcranial magnetic stimulation (Farzan et al., 2016), as well as neuropsychological assessments of the CCAS (Molinari et al., 2008, Schmahmann and Sherman, 1998), including modifications in behavior resulting from theta burst stimulation (Del Olmo et al., 2007).

The theory of the UCT holds that a singular mechanism emerges from an essentially uniform cerebellar anatomy, and performs its computation on different channels of information processing subserved by anatomically precise connections linking focal cerebellar regions with different cerebral areas. This enables the UCT to manifest as different functions, from movement coordination to cognition and emotion. In this view, different functions of the UCT (inferred from behavioral observations and guided by motor analogies, e.g., the regulation of rate, rhythm and accuracy of movement, and therefore the regulation of speed, capacity, consistence and appropriateness of emotions [Schmahmann, 1991]) would be understood as different manifestations of the common mechanism.

Examples abound in nature by which a common mechanism performs multiple functions depending on its environment or location. Cells use polypeptides in different ways by locating them in different environments. This is exemplified by the functions of the enzyme glyceraldehyde-3-phosphate dehydrogenase which include DNA repair, tRNA export, membrane fusion and transport, and cytoskeletal dynamics – depending on its location (Sirover, 2011). Language function can also change depending on the environment (“Think of exclamations, with their completely different functions: “No!”, or “Water!”” [Wittgenstein, 1953]). In the cerebellum, because of its connections with different areas of the cerebral hemispheres, the UCT operates in different environments and therefore manifests as different functions. In this view, regional differences in function resulting from cerebellar modulation (the UCT) emerge from the heterogeneity of its connectivity, i.e., differences in environment/location, rather than from variation in cerebellar cytoarchitecture or physiology.

Confirmation of the UCT would guide the definition of the functions of the cerebellum. If cerebellar functions are shown to emerge from a common mechanism (the UCT), cerebellar functions are expected to share common underlying principles. As a consequence, definition of one cerebellar function will guide the definition of other cerebellar functions. Thus, if cerebellar damage impairs the rate, rhythm and accuracy of movement, the logical inference by analogy is that the cerebellum contributes to affect by regulating the speed, capacity, consistence and appropriateness of emotions (Schmahmann, 1991). Additionally, evidence supporting the existence of a UCT would facilitate research into the mechanism of the cerebellum since it would guide future investigations to focus on the description of one single mechanism underlying all cerebellar functions. A recent review article (Sokolov et al., 2017) provides a somewhat analogous argument: “If principles of information processing are indeed similar across the cerebellum, we should consider mechanistic hypotheses that would be consistent across task domains. Hence, our understanding of cerebellar involvement in cognition may benefit from considering the substantial knowledge we have on how the cerebellum contributes to sensorimotor control”. We would add that, therefore, there is a need for future research to directly test the UCT hypothesis. Accordingly, we would include “Is there a Universal Cerebellar Transform?” as one of the outstanding questions presented in Sokolov et al., 2017.

Better understanding of the mechanism and functions of the cerebellum facilitated by the confirmation of the UCT theory could potentially impact the understanding, diagnosis and treatment of the ataxias as well as other diseases where cerebellar structural and functional abnormalities have been identified; such as major depressive disorder, anxiety disorders, bipolar disorder, schizophrenia, attention deficit and hyperactivity disorder, and autism spectrum disorders (for a review, see Phillips, Hewedi, Eissa, & Moustafa, 2015).

There is therefore a great need to directly test the UCT hypothesis, as well as to explore its relationship with the next step in the evolution of standard cognitive science (Wheeler, 2005) – embodied cognition. The following sections will provide novel insights into the relationship between embodiment and the UCT theory.