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Erroneous sensorimotor processing in functional disorders. evidence from gaze motor control of functional dizziness and irritable bowel patients
Erroneous sensorimotor processing in functional disorders. evidence from gaze motor control of functional dizziness and irritable bowel patients
Patients with functional disorders suffer from persistent somatic symptoms that are insufficiently explained by an organic dysfunction. Such symptoms are common in medicine and can be strongly debilitating for the affected persons. Yet, our current understanding about the underlying pathophysiology is still sparse, challenging diagnosis and therapy in this underserved patient group. A recently evolved theoretical framework based on the concept of predictive processing describes the emergence and manifestation of functional disorders as a consequence of processing deficits in the central nervous system. Here, prior knowledge and expectations are thought to bias sensory signal processing towards a pathological direction, so that emerging symptom percepts are uncoupled from organ functioning and corresponding sensory input. As so far, empirical evidence confirming this theory is still sparse, the aim of the current thesis was to experimentally investigate the role of expectations in sensorimotor processing of patients with functional disorders. For this purpose, patients with functional dizziness and irritable bowel syndrome (IBS), i.e., functional gastrointestinal symptoms, were investigated in a gaze shift paradigm. In this paradigm, eye-head gaze shifts are performed under normal head properties and with increased head moment of inertia. The experimental perturbation induces a mismatch between the intended and executed head movement, so that the expected and actual sensory consequences of the head movement do not match. Adaptation to this new context allows conclusions about a correct use of expectations and sensory input during sensorimotor processing. Study 1 investigated patients with functional dizziness and a healthy control group in the gaze shift paradigm. Sensorimotor processing was analyzed by assessing head oscillations. They arise when the increased head moment of inertia is not (yet) incorporated in internal models of the head and accounted for in motor planning. Head oscillations were higher in patients with functional dizziness than in the healthy control group, indicating sensorimotor processing deficits that prevent adaptation to the altered head properties. Such deficits were already found, to a smaller extent, in the natural condition. By reanalyzing data from patients with organic dizziness performing the same experiment, i.e., bilateral vestibulopathy and cerebellar ataxia, no difference could be found between the height of head oscillations in these patient groups and in functional dizziness, demonstrating similar impairment. In study 2, gaze stability of patients with functional dizziness and a healthy control group was analyzed during gaze shifts in the paradigm described above. Patients showed impaired gaze stability during a distinct epoch of the large gaze shift, in which gaze was stabilized against active head movements. In this epoch, information from motor planning and internal models can be used additionally to ongoing sensory input to stabilize gaze. In contrast, during another epoch of the gaze shift, in which gaze was stabilized against passive, unexpected head movements by using sensory input alone, gaze stabilization was intact. These results further revealed sensorimotor processing deficits in functional dizziness, this time in the functionally relevant parameter of the task, i.e., gaze. Here, processing deficits arise due to an incorrect use of expectations. They were already present in the natural condition, and further pronounced with increased head moment of inertia. The third study investigated patients with IBS and a healthy control group in the gaze shift paradigm to look for generalized, symptom-unspecific processing deficits that manifest across organ systems. Patients with IBS showed difficulties in adapting to the new context of increased head moment of inertia, reflected in increased head oscillations. These results point at transdiagnostic processing deficits. As head oscillations in patients with IBS were smaller than in patients with functional dizziness, these processing alterations might represent a risk factor for developing further functional symptoms rather than representing a measurable correlate of pathophysiology. Together, the findings of the presented studies provide evidence for the predictive processing account of functional disorders, pointing at incorrect expectations that bias sensorimotor processing and impair adaptation in the gaze shift paradigm. Identifying measurable pathophysiological correlates (study 1 and 2) and unifying deficits across symptom modalities (study 3) enhances our understanding of functional disorders and has the potential to improve diagnosis and therapy in this patient group.
Not available
Schröder, Lena
2023
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Schröder, Lena (2023): Erroneous sensorimotor processing in functional disorders: evidence from gaze motor control of functional dizziness and irritable bowel patients. Dissertation, LMU München: Graduate School of Systemic Neurosciences (GSN)
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Abstract

Patients with functional disorders suffer from persistent somatic symptoms that are insufficiently explained by an organic dysfunction. Such symptoms are common in medicine and can be strongly debilitating for the affected persons. Yet, our current understanding about the underlying pathophysiology is still sparse, challenging diagnosis and therapy in this underserved patient group. A recently evolved theoretical framework based on the concept of predictive processing describes the emergence and manifestation of functional disorders as a consequence of processing deficits in the central nervous system. Here, prior knowledge and expectations are thought to bias sensory signal processing towards a pathological direction, so that emerging symptom percepts are uncoupled from organ functioning and corresponding sensory input. As so far, empirical evidence confirming this theory is still sparse, the aim of the current thesis was to experimentally investigate the role of expectations in sensorimotor processing of patients with functional disorders. For this purpose, patients with functional dizziness and irritable bowel syndrome (IBS), i.e., functional gastrointestinal symptoms, were investigated in a gaze shift paradigm. In this paradigm, eye-head gaze shifts are performed under normal head properties and with increased head moment of inertia. The experimental perturbation induces a mismatch between the intended and executed head movement, so that the expected and actual sensory consequences of the head movement do not match. Adaptation to this new context allows conclusions about a correct use of expectations and sensory input during sensorimotor processing. Study 1 investigated patients with functional dizziness and a healthy control group in the gaze shift paradigm. Sensorimotor processing was analyzed by assessing head oscillations. They arise when the increased head moment of inertia is not (yet) incorporated in internal models of the head and accounted for in motor planning. Head oscillations were higher in patients with functional dizziness than in the healthy control group, indicating sensorimotor processing deficits that prevent adaptation to the altered head properties. Such deficits were already found, to a smaller extent, in the natural condition. By reanalyzing data from patients with organic dizziness performing the same experiment, i.e., bilateral vestibulopathy and cerebellar ataxia, no difference could be found between the height of head oscillations in these patient groups and in functional dizziness, demonstrating similar impairment. In study 2, gaze stability of patients with functional dizziness and a healthy control group was analyzed during gaze shifts in the paradigm described above. Patients showed impaired gaze stability during a distinct epoch of the large gaze shift, in which gaze was stabilized against active head movements. In this epoch, information from motor planning and internal models can be used additionally to ongoing sensory input to stabilize gaze. In contrast, during another epoch of the gaze shift, in which gaze was stabilized against passive, unexpected head movements by using sensory input alone, gaze stabilization was intact. These results further revealed sensorimotor processing deficits in functional dizziness, this time in the functionally relevant parameter of the task, i.e., gaze. Here, processing deficits arise due to an incorrect use of expectations. They were already present in the natural condition, and further pronounced with increased head moment of inertia. The third study investigated patients with IBS and a healthy control group in the gaze shift paradigm to look for generalized, symptom-unspecific processing deficits that manifest across organ systems. Patients with IBS showed difficulties in adapting to the new context of increased head moment of inertia, reflected in increased head oscillations. These results point at transdiagnostic processing deficits. As head oscillations in patients with IBS were smaller than in patients with functional dizziness, these processing alterations might represent a risk factor for developing further functional symptoms rather than representing a measurable correlate of pathophysiology. Together, the findings of the presented studies provide evidence for the predictive processing account of functional disorders, pointing at incorrect expectations that bias sensorimotor processing and impair adaptation in the gaze shift paradigm. Identifying measurable pathophysiological correlates (study 1 and 2) and unifying deficits across symptom modalities (study 3) enhances our understanding of functional disorders and has the potential to improve diagnosis and therapy in this patient group.