Changes in excitability of ascending and descending inputs to cerebellar climbing fibers during locomotion.

The inferior olive climbing fiber projection plays a central role in all major theories of cerebellar function. Therefore, mechanisms that control the ability of climbing fibers to forward information to the cerebellum are of considerable interest. We examined changes in transmission in cerebro-olivocerebellar pathways (COCPs) and spino-olivocerebellar pathways (SOCPs) during locomotion in awake cats (n = 4) using low-intensity electrical stimuli delivered to the contralateral cerebral peduncle or the ipsilateral superficial radial nerve to set up volleys in COCPs and SOCPs, respectively. The responses were recorded as evoked extracellular climbing fiber field potentials within the C1 or C3 zones in the paravermal cerebellar cortex (lobule Va-Vc). At most C1 and C3 zone sites, the largest COCP responses occurred during the stance phase, and the smallest responses occurred during the swing phase of the ipsilateral forelimb step cycle. In marked contrast, SOCP responses recorded at the same sites were usually largest during the swing phase and smallest during the stance phase. Because substantial climbing fiber responses could be evoked in all phases of the step cycle, the results imply that olivary neurons remain excitable throughout, and that the differences between SOCPs and COCPs in their pattern of step-related modulation are unlikely to have arisen solely through inhibition at the level of the inferior olive (e.g., by activity in the inhibitory cerebellar nucleo-olivary pathway). The different patterns of modulation also suggest that climbing fiber signals conveyed by COCPs and SOCPs are likely to affect information processing within the cerebellar cortical C1 and C3 zones at different times during locomotion.