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Quantitative evaluation of posture control in rats with inferior olive lesions.

ABSTRACT: Impairment of inferior olivary neurons (IONs) affects whole-body movements and results in abnormal gait and posture. Because IONs are activated by unpredicted motion rather than regular body movements, the postural dysfunction caused by ION lesions is expected to involve factors other than simple loss of feedback control. In this study, we measured the postural movements of rats with pharmacological ION lesions (IO rats) trained to stand on their hindlimbs. The coordination of body segments as well as the distribution and frequency characteristics of center of mass (COM) motion were analyzed. We determined that the lesion altered the peak properties of the power spectrum density of the COM, whereas changes in coordination and COM distribution were minor. To investigate how the observed properties reflected changes in the control system, we constructed a mathematical model of the standing rats and quantitatively identified the control system. We found an increase in linear proportional control and a decrease in differential and nonlinear control in IO rats compared with intact rats. The dystonia-like changes in body stiffness explain the nature of the linear proportional and differential control, and a disorder in the internal model is one possible cause of the decrease in nonlinear control.

SUBMITTER: Funato T

PROVIDER: S-EPMC8514513 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Quantitative evaluation of posture control in rats with inferior olive lesions.

Funato Tetsuro T Sato Yota Y Sato Yamato Y Fujiki Soichiro S Aoi Shinya S Tsuchiya Kazuo K Yanagihara Dai D

Scientific reports 20211013 1

Impairment of inferior olivary neurons (IONs) affects whole-body movements and results in abnormal gait and posture. Because IONs are activated by unpredicted motion rather than regular body movements, the postural dysfunction caused by ION lesions is expected to involve factors other than simple loss of feedback control. In this study, we measured the postural movements of rats with pharmacological ION lesions (IO rats) trained to stand on their hindlimbs. The coordination of body segments as w ...[more]

PMID: 34645901

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Project description:We previously proposed, on theoretical grounds, that the cerebellum must regulate the dimensionality of its neuronal activity during motor learning and control to cope with the low firing frequency of inferior olive neurons, which form one of two major inputs to the cerebellar cortex. Such dimensionality regulation is possible via modulation of electrical coupling through the gap junctions between inferior olive neurons by inhibitory GABAergic synapses. In addition, we previously showed in simulations that intermediate coupling strengths induce chaotic firing of inferior olive neurons and increase their information carrying capacity. However, there is no in vivo experimental data supporting these two theoretical predictions. Here, we computed the levels of synchrony, dimensionality, and chaos of the inferior olive code by analyzing in vivo recordings of Purkinje cell complex spike activity in three different coupling conditions: carbenoxolone (gap junctions blocker), control, and picrotoxin (GABA-A receptor antagonist). To examine the effect of electrical coupling on dimensionality and chaotic dynamics, we first determined the physiological range of effective coupling strengths between inferior olive neurons in the three conditions using a combination of a biophysical network model of the inferior olive and a novel Bayesian model averaging approach. We found that effective coupling co-varied with synchrony and was inversely related to the dimensionality of inferior olive firing dynamics, as measured via a principal component analysis of the spike trains in each condition. Furthermore, for both the model and the data, we found an inverted U-shaped relationship between coupling strengths and complexity entropy, a measure of chaos for spiking neural data. These results are consistent with our hypothesis according to which electrical coupling regulates the dimensionality and the complexity in the inferior olive neurons in order to optimize both motor learning and control of high dimensional motor systems by the cerebellum.

Project description:The inferior olive (IO) is a neural network belonging to the olivo-cerebellar system whose neurons are coupled with electrical synapses and display subthreshold oscillations and spiking activity. The IO is frequently proposed as the generator of timing signals to the cerebellum. Electrophysiological and imaging recordings show that the IO network generates complex spatio-temporal patterns. The generation and modulation of coherent spiking activity in the IO is one key issue in cerebellar research. In this work, we build a large scale IO network model of electrically coupled conductance-based neurons to study the emerging spatio-temporal patterns of its transient neuronal activity. Our modeling reproduces and helps to understand important phenomena observed in IO in vitro and in vivo experiments, and draws new predictions regarding the computational properties of this network and the associated cerebellar circuits. The main factors studied governing the collective dynamics of the IO network were: the degree of electrical coupling, the extent of the electrotonic connections, the presence of stimuli or regions with different excitability levels and the modulatory effect of an inhibitory loop (IL). The spatio-temporal patterns were analyzed using a discrete wavelet transform to provide a quantitative characterization. Our results show that the electrotonic coupling produces quasi-synchronized subthreshold oscillations over a wide dynamical range. The synchronized oscillatory activity plays the role of a timer for a coordinated representation of spiking rhythms with different frequencies. The encoding and coexistence of several coordinated rhythms is related to the different clusterization and coherence of transient spatio-temporal patterns in the network, where the spiking activity is commensurate with the quasi-synchronized subthreshold oscillations. In the presence of stimuli, different rhythms are encoded in the spiking activity of the IO neurons that nevertheless remains constrained to a commensurate value of the subthreshold frequency. The stimuli induced spatio-temporal patterns can reverberate for long periods, which contributes to the computational properties of the IO. We also show that the presence of regions with different excitability levels creates sinks and sources of coordinated activity which shape the propagation of spike wave fronts. These results can be generalized beyond IO studies, as the control of wave pattern propagation is a highly relevant problem in the context of normal and pathological states in neural systems (e.g., related to tremor, migraine, epilepsy) where the study of the modulation of activity sinks and sources can have a potential large impact.

Project description:BackgroundConservative treatment in the adolescent idiopathic scoliosis (AIS) population is based on individual proprioceptive and motor control training. Such training includes physiotherapeutic scoliosis-specific exercises (PSSEs) stimulating the individual capacity to perceive and control his/her posture, particularly the shape of the spine. However, limited knowledge about basic proprioception capability in AIS patients is reported in the literature.Questions(1) How do AIS patients, who did not receive any previous specific postural education treatment, perceive their posture and 3D spine shape? Are they able to modify their posture and 3D spine shape correctly through an instinctive self-correction (ISCO) maneuver? (2) Are posture and ISCO maneuver ability gender dependent in AIS patients? (3) Do AIS patients present different posture and spine shape characteristics as well as different ISCO ability compared with the healthy young adult population?MethodsCross-sectional observational study. 132 (75 females, 57 males) AIS patients' posture and 3D spine shape have been measured comparing indifferent orthostasis (IO) (neutral erect posture) to ISCO using a non-ionizing 3D optoelectronic stereophotogrammetric approach. Thirteen quantitative biomechanical parameters described the AIS patients body posture. The statistical analysis was performed using a multivariate approach to compare genders in IO, ISCO, and AIS patients vs. healthy young adults-previously published data (57 females, 64 males).ResultsMales (87.7%) and females (93.3%) of AIS patients were unable to modify posture and 3D spine shape globally. AIS patients gender differences were found in IO, ISCO, and the comparison vs. healthy young adults. When changes occurred, subjects could not focus and control their posture globally, but only in a few aspects at a time.ConclusionSelf-correction maneuver producing an improvement in body posture and spine shape is not instinctive and must be trained. In such characteristics, AIS patients are not so dissimilar to healthy young adults. Sagittal plane control is the highest, but ISCO in AIS patients led to worsening in this plane. Control at the lumbar level is neglected in both genders. Such outcomes support the necessity of customized PSSEs to treat AIS patients. The 3D stereo-photogrammetric approach is effective in quantitatively describing the subject's posture, motor control, and proprioception.

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Quantitative evaluation of posture control in rats with inferior olive lesions.

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Quantitative evaluation of posture control in rats with inferior olive lesions.

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