The role of the cerebellum in affect and psychosis

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Abstract

Anatomical, clinical, and functional imaging studies suggest that the cerebellum is an essential component of the distributed neural circuitry subserving cognition. This paper addresses the experimental and clinical data pointing to the role of the cerebellum in the modulation of affect and emotion as well as of thought. There are cerebellar connections with the reticular system (arousal), hypothalamus (autonomic function and emotional expression), limbic system (experience and expression of emotion), and paralimbic and neocortical association areas (cognitive dimensions of affect). Clinical studies point to cerebellar modulation of aggression and mood, including the cerebellar cognitive affective syndrome in adults and children, the posterior fossa syndrome of transient mutism and behavioral change following surgery that involves the vermis, and behavioral modification by cerebellar neurosurgical manipulation. Functional imaging studies reveal cerebellar involvement in nociception, in autonomic behaviors such as hunger and thirst, and in affective experiences. These observations provide support for the hypothesis that the cerebellum is an essential node in the distributed neural circuitry subserving cognitive and affective functions, and that there is a topographic organization of behaviors in the cerebellum. The hypothesis that the phylogenetically older fastigial nucleus, vermis and flocculonodular lobe constitute the “limbic cerebellum” is further developed to suggest that these cerebellar structures should be considered an extension of the Papez circuit. The concept is proposed that there is a universal cerebellar transform (UCT), possibly error detection, prevention, and correction utilizing an internal model, the disruption of which leads to dysmetria, the universal cerebellar impairment (UCI). Dysmetria of movement, or ataxia, is matched by dysmetria of thought, including the cerebellar cognitive affective syndrome, abnormalities of affect, and psychotic thinking.

Introduction

Contemporary investigations provide substantial clinical and experimental support for the hypothesis generated in the early part of the 20th century that the cerebellum participates in a multitude of nervous system functions beyond that of motor control. This paper explores the observations and hypotheses that have, until recently, been less influential than the “motor cerebellum” school of thought. It summarizes anatomic investigations demonstrating substrates that could sustain a cerebellar contribution to nonmotor as well as motor behaviors, and describes contemporary clinical studies that report changes in behavior, personality and affect following lesions of the cerebellum. It includes data from morphologic and functional neuroimaging experiments that support a wider role of the cerebellum in nervous system function, and specifically that suggest an important contribution of the cerebellum to the regulation of affect and to psychosis. The paper concludes with an examination of the dysmetria of thought hypothesis, and discusses how this theory harmonizes with models of cerebellar function proposed by other contemporary theorists. Our thesis is that the cerebellum is an essential node in the distributed neural circuitry subserving cognitive and affective functions as well as other functions traditionally thought to be under cerebellar influence; that there is a topographic organization of behaviors in the cerebellum and that the phylogenetically older fastigial nucleus, vermis and flocculonodular lobe are the “limbic cerebellum”; and that the study of cerebellum may provide new insights into instinctive behaviors and disorders of emotion and thought.

Section snippets

Affect and emotion — a definition

The term “affect” was originally used by Freud [1] to denote the signal of some kind of danger to one’s self-regard and existence. The term has been used more generally for some time, however [2], [3], to imply a mood state, both as it is subjectively experienced and in its outward manifestations. Affect is embedded within the complex phenomenon of emotion that draws on multiple anatomic and physiologic substrates. As part of the essential behavioral repertoires of all mammals, emotions serve

Early accounts

Luigi Rolando [5] demonstrated that cerebellar lesions produced aberrations of movement, but Marie-Jean-Pierre Flourens [6] concluded that the principal result of cerebellar extirpation was impairment of muscular coordination. Of considerable interest, however, is the following observation of Flourens, “in all the animals and at all ages, slight interference with the cerebellum always causes a slight lack of coordination of movement which always increases with the interference; and the total

Three hierarchical systems supporting behavior and affect

Experimental observations in three different hierarchically organized behaviors and anatomic systems heralded the scientific journey into the domain of a cerebellar contribution to affect. First, there were early indicators of a connection in the cat between cerebellum and arousal. These included descriptions by Moruzzi and Magoun [14] of flattening of the electroencephalographic pattern by fastigial nucleus stimulation, of Snider et al. [15] that single shock stimulation of the culmen or

Further behavioral observations

Snider and Stowell [38] recorded electrical potentials in the cerebellum of a cat following cutaneous stimulation of the periphery and following visual stimuli (flashing lights) and auditory stimuli (clicking sound). In addition they observed that stimulation of the cerebral cortex in auditory and visual regions produced cerebellar potentials in regions that overlap those resulting from the peripheral stimulation. These seminal observations led to two main conclusions. First, there was

Anatomic substrates

“Is emotion a magic product or is it a physiologic process which depends on an anatomic mechanism?” In attempting to answer his question, Papez [4] proposed “that the hypothalamus, the anterior thalamic nuclei, the gyrus cinguli, the hippocampus, and their interconnections constitute a harmonious mechanism which may elaborate the functions of central emotion, as well as participate in emotional expression.” The limbic system as defined by Papez has been shown in clinical and experimental

Clinical observations

Against the background of the early clinical observations, experimental investigations, and the consideration of anatomic substrates that could subserve a cerebellar contribution to affect, it is useful to consider the contemporary systematic clinical reports that have addressed the nature of the affective disturbances resulting from cerebellar lesions and that have brought forth a credible challenge to established notions in psychiatry and neurology by postulating a cerebellar role in the

Neuroimaging observations

Positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) have revealed cerebellar activation by tasks within multiple cognitive domains including executive, linguistic, mnemonic, attentional and visual/spatial functions in addition to sensorimotor paradigms. There appears to be a functional topography within cerebellum as suggested by a meta-analysis of published studies charted onto a semi-flattened map of the human cerebellar cortex [103] derived from the three

Synthesis and hypothesis

There is increasing evidence that in the functional and clinical domains the cerebellar role in the nervous system extends considerably beyond the conventional notion of motor control, and that indeed, control of motor performance is but one of a multitude of functions subserved by the cerebellum (in the same way as motor performance is but one of a multitude of functions subserved by the cerebral hemispheres).

The prerequisites for emotional experience and expression include arousal, autonomic,

Acknowledgements

This work was supported in part by a grant from the James S. McDonnell Foundation. The constructive reviews of the manuscript by Lawrence M. Parsons, PhD and Deepak N. Pandya, MD are gratefully acknowledged.

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