Olivo-cerebellar cluster-based universal control system

Abstract

The olivo-cerebellar network plays a key role in the organization of vertebrate motor control. The oscillatory properties of inferior olive (IO) neurons have been shown to provide timing signals for motor coordination in which spatio-temporal coherent oscillatory neuronal clusters control movement dynamics. Based on the neuronal connectivity and electrophysiology of the olivo-cerebellar network we have developed a general-purpose control approach, which we refer to as a universal control system (UCS), capable of dealing with a large number of actuator parameters in real time. In this UCS, the imposed goal and the resultant feedback from the actuators specify system properties. The goal is realized through implementing an architecture that can regulate a large number of parameters simultaneously by providing stimuli-modulated spatiotemporal cluster dynamics.T he olivo-cerebellar system, one of the key neuronal circuits in the brain, has been shown to provide highly coordinated signals concerned with the temporal organization of movement execution (1-3). This neuronal network involves inferior olive (IO) neurons whose axons, the climbing fibers, terminate as excitatory inputs onto Purkinje cells in the cerebellar cortex and as en-passant collaterals onto the cerebellar nuclear neurons. The Purkinje cells, in turn, exert a powerful synaptic inhibition onto these cerebellar nuclear neurons (4). Much of the intrinsic activity in this network is supported by autonomous subthreshold membrane potential oscillations in IO neurons that display a close-to 10-Hz frequency (5-7). Action potentials in IO neurons occur at the depolarization apex of these oscillations (5).To implement motor coordination via the olivo-cerebellar system, the IO nucleus is organized such that the dendrites of the IO neurons are electrotonically coupled (8, 9) via dendritic gap junctions (10) and receive inhibitory feedback from the cerebellar nuclei (11)(12)(13)(14). It was originally proposed that this inhibitory input produced a dynamic decoupling of the IO neurons (9). This finding was later demonstrated to be correct by using multiple electrode recordings at the cerebellar cortex (15). Thus, the coupling serves to synchronize the oscillatory phase of IO neurons whereas the return nuclear inhibition, by transiently shunting dendritic coupling, controls cluster size and contour. The interplay between these two processes provides the pattern formation responsible for motor control via ''cluster dynamics'' in the IO (16). Such functional clusters have been demonstrated in vitro by using voltage-dependent dye imaging of the IO (16) and in vivo at the Purkinje cell layer by using multiple electrode recordings (17, 18). The temporal dynamics of the cluster activity have been shown to be directly correlated with premotor temporal patterns of Purkinje cell activity during motor execution (19).The control complexity that the CNS must implement to execute movements as simple as merely grasping an object requires the simultaneous activation of 50 key mu...

Self-referential phase reset based on inferior olive oscillator dynamics

“…Because spike threshold occurs mostly at the peak of a subthreshold oscillation, spike onset is determined by the subthreshold oscillation. Depending on the values of the control parameters, the model qualitatively reproduces the spontaneous and stimuli-induced oscillations observed in IO neurons (8,15). A mathematical model comprising a set of four nonlinear differential equations can describe these properties:…”

“…We have developed a mathematical model that reproduces the key IO neuron electrophysiological properties (8,15) and the SPR effect. In particular, the model comprises two sets of functionally coupled equations where the oscillations of Abbreviations: IO, inferior olive; SPR, self-referential phase reset.…”

“…During the short time IO neurons are electrically uncoupled, they may receive direct sensory feedback that can provide the desired cluster configuration. The olivocerebellar cluster-based universal control system (UCS) has been described in detail (8). SPR-induced synchronization as implemented with the UCS architecture is illustrated in Fig.…”

“…Recent experimental work indicates that such a temporal signal mechanism is provided by the sequence of oscillatory events in the olivo-cerebellar system (7). The possibility that a ''universal control system,'' based on olivo-cerebellar physiology, may be implemented in analog hardware electronic chips has been proposed (8).…”

Improvements in Quality of Life in Individuals with Friedreich’s Ataxia after Participation in a 5-Year Program of Physical Activity: An observational Study Pre-Post Test Design, and Two Years Follow-Up

“…There is considerable evidence to support the network perspective for describing and explaining brain function, giving rise to theories such as the universal control system, [34] and the concept of synaptic homoeostasis for the stabilization of neuronal circuits [35]. One of the things we know about neural plasticity is that it is enhanced by new behavioral learning, rather than just repetition of exercises/activities in the absence of learning [36], supporting the hypothesis that's implemotor activity is insufficient to produce long-term plasticity in cortical representations.…”