Error detection and representation in the olivo-cerebellar system

Abstract

Complex spikes generated in a cerebellar Purkinje cell via a climbing fiber have been assumed to encode errors in the performance of neuronal circuits involving Purkinje cells. To reexamine this notion in this review, I analyzed structures of motor control systems involving the cerebellum. A dichotomy was found between the two types of error: sensory and motor errors play roles in the feedforward and feedback control conditions, respectively. To substantiate this dichotomy, here in this article I reviewed recent data on neuronal connections and signal contents of climbing fibers in the vestibuloocular reflex (VOR), optokinetic eye movement response, saccade, hand reaching, cursor tracking, as well as some other cases of motor control. In our studies, various sources of sensory and motor errors were located in the neuronal pathways leading to the inferior olive. We noted that during the course of evolution, control system structures involving the cerebellum changed rather radically from the prototype seen in the flocculonodular lobe and vermis to that applicable to the cerebellar hemisphere. Nevertheless, the dichotomy between sensory and motor errors is maintained.

Keywords: adaptation; error; internal model; microcomplex; motor learning.

Figure 1

Two types of adaptive control system. (A) Without online feedback. (B) With online feedback. Pathways for computing error signals are indicated by red lines.

Figure 2

Basic circuit structure of microcomplex. Abbreviations: CF, climbing fiber; GR, granule cell; IO, inferior olive; MF, mossy fiber; NN/VN, nuclear neuron/vestibular nuclear neuron; no, nucleoolivary pathway; nro, nucleorubroolivary pathway; PC, Purkinje cell; PCN, precerebellar neuron; PF, parallel fiber; pRN, parvocellular red nucleus; eNN, excitatory nuclear neuron; iNN, inhibitory nuclear neuron; ro, rubroolivary pathway; nr, nucleorubral pathway Inhibitory neurons are in black (others are excitatory).

Figure 3

Two types of internal model. (A) Forward model linked to feedforward controller. (B) Inverse model linked to feedback controller.

Figure 4

Control system structure for three types of eye movement reflex. (A) VOR. (B) OKR. (C) saccade. Additional abbreviations: β, β subnucleus of inferior olive; DC, dorsal cap; EM, extraocular muscle; FA, fastigial nucleus; NRTP, nucleus reticularis tegmenti pontis; OKS, optokinetic stimulus; OM, oculomotor neurons; SC, superior colliculus; SG, saccade generator; AOS, accessory optic system; FL, flocculus; VN, vestibular nuclear neuron; MC, microcomplex; VO, vestibular organ; PV, posterior vermis; x, vestbuloocular relay neuron; y, vestibular nuclear neuron working in parallel with x.

Figure 5

Models for voluntary motor control. (A) Forward-model-based control of arm movement by primary motor cortex. (B) Inverse-model-based control. (C) Application of reflex control scheme. Additional abbreviations: ccc, cerebrocerebellar communication loop. CO, control object including segmental circuit and skeletomuscular system; MC, microcomplex, M1, primary motor cortex; IO, inferior olive; Ip, instructed performance; Rp, realized performance; ro, rubroolivary pathway; pRN, parvocellular red nucleus; nr, nucleorubral pathway.