Fig. 9.23 ). The spontaneous simple spike firing rate of a Purkinje cell typically is between 20 and 100 Hz but can be modulated over a much wider range (from 0 to >200 Hz), depending on the relative balance of excitation from parallel fiber input and inhibition from cerebellar cortex interneurons. Thus this activity reflects the state of the cerebellar cortex. Interestingly, evidence from studies performed in the early 2000s indicates that the spontaneous levels of simple spike activity vary systematically across the cerebellar cortex: Firing rates in zebrin-negative regions average twice those of the zebrin-positive regions. The full significance of this discovery is not known, but it suggests that despite the anatomical uniformity of the cerebellar cortical circuits, they might be functionally quite distinct.
•Fig. 9.23 Responses of a Purkinje Cell to Excitatory Input, Recorded Extracellularly. A, Granulecells,viatheirascendingaxonsandparallelfibers,excitePurkinjecellsandtriggersimplespikes.B, Climbingfiberactivityleadstohigh-frequency(≈500-Hz)burstsofspikesknownascomplex spikes inPurkinjecells.Notethatthespikesfollowingtheinitialonearesmallerandreferredtoasspikelets.
In contrast, a climbing fiber discharge causes a high-frequency burst of action potentials, called a complex spike (see
Fig. 9.23 ), in an all-or-none manner because of the massive excitation that is provided by the single climbing fiber that a Purkinje cell receives. This excitation is so powerful that there is essentially a one-to-one relationship between climbing fiber discharge and a complex spike. Thus complex spikes essentially override what is happening at the cortex level and reflect the state of the inferior olivary nucleus. The average firing rate of a spontaneous complex spike is only about 1 Hz.
Because the climbing fibers generate complex spikes at such a low frequency, they do not substantially change the average firing rates of Purkinje cells, and as a consequence, it is commonly argued that they have no direct role in shaping the output of the cerebellar cortex and are therefore not involved in ongoing motor control. Instead, it is commonly thought that their function is to alter the responsiveness of Purkinje cells to parallel fiber input. In particular, under certain circumstances, complex spike activity produces a prolonged depression in synaptic efficacy of parallel fibers, termed long-term depression (LTD). This phenomenon is the proposed mechanism by which climbing fibers act in motor-learning hypotheses. According to typical hypotheses about it, the parallel fiber system and hence simple spikes are involved in generating ongoing movement, and when there is a mismatch between the intended and actual movement, this error activates the inferior olivary nucleus and complex spikes result, which then lead to LTD of the active parallel fiber synapses. This adjustment in synaptic weight changes the motor output in the future. If this change results in a properly executed movement, activation of the inferior olivary nucleus does not occur, and the motor program is unchanged, but if there is still an error, the olivocerebellar system triggers additional complex spikes that cause further changes in synaptic efficacy, and so on. Major challenges to this view are that motor learning can occur when LTD is chemically blocked and that learned behavior can remain after removal of portions of the cerebellum in which the memory is supposedly stored.