Patterns of Spontaneous Purkinje Cell Complex Spike Activity in the Awake Rat

Abstract

The olivocerebellar system is known to generate periodic synchronous discharges that result in synchronous (to within 1 msec) climbing fiber activation of Purkinje cells (complex spikes) organized in parasagittally oriented strips. These results have been obtained primarily in anesthetized animals, and so the question remains whether the olivocerebellar system generates such patterns in the awake animal. To this end, multiple electrode recordings of crus 2a complex spike activity were obtained in awake rats conditioned to execute tongue movements in response to a tone. After removal of all movementand tone-related activity, the remaining data were examined to characterize spontaneous complex spike activity in the alert animal. Spontaneous complex spikes occurred at an average firing rate of 1 Hz and a clear Ϸ10 Hz rhythmicity. Analysis of the autocorrelograms using a rhythm index indicated that the large majority of Purkinje cells displayed rhythmicity, similar to that in the anesthetized preparation. In addition, the patterns of synchronous complex spike activity were also similar to those observed in the anesthetized preparation (i.e., simultaneous activity was found predominantly among Purkinje cells located within the same parasagittally oriented strip of cortex). The results provide unequivocal evidence that the olivocerebellar system is capable of generating periodic patterns of synchronous activity in the awake animal. These findings support the extrapolation of previous results obtained in the anesthetized preparation to the waking state and are consistent with the timing hypothesis concerning the role of the olivocerebellar system in motor coordination.

Role of Myelination in the Development of a Uniform Olivocerebellar Conduction Time

“…The olivocerebellar system generates synchronous, on a millisecond time scale, CS activity (Lang et al 1999;Llinás and Sasaki 1989;Sasaki et al 1989;Wylie et al 1995). The ability to generate synchronous activity has long been ascribed to the electrotonic coupling of IO neurons by gap junctions (Llinás 1974;Llinás et al 1974).…”

“…In the rat, the distance between the IO and the cortex can vary by almost twofold (Sugihara et al 1993). However, synchronous CS activity does occur (Lang et al 1999;Llinás and Sasaki 1989;Sasaki et al 1989;Wylie et al 1995), even between widely separated regions of the cortex because of mechanisms that allow a uniform conduction time across the cerebellum (De Zeeuw et al 1996).…”

“…Indeed, the density of neuronal gap junctions appears to be higher in the IO than in any other CNS region (Belluardo et al 2000;Condorelli et al 1998;De Zeeuw et al 1995). This coupling allows IO neurons to generate precisely (on a millisecond time scale) synchronized activity that results in simultaneous complex spike (CS) activity in the cerebellum (Lang et al 1999;Sasaki et al 1989;Sugihara et al 1993;Yamamoto et al 2001).…”

“…Indeed, the density of neuronal gap junctions appears to be higher in the IO than in any other CNS region (Belluardo et al 2000;Condorelli et al 1998;De Zeeuw et al 1995). This coupling allows IO neurons to generate precisely (on a millisecond time scale) synchronized activity that results in simultaneous complex spike (CS) activity in the cerebellum (Lang et al 1999;Sasaki et al 1989;Sugihara et al 1993;Yamamoto et al 2001).Maintenance of the synchronization present in IO discharges presents a challenge for the olivocerebellar system because the length of the olivocerebellar pathway to different points on the cerebellar cortex varies. In rats, there can be more than a twofold difference in the length of the olivocerebellar projection to different regions of the cortex (Sugihara et al 1993).…”

A possible role of olivary gap-junctions in the generation of physiological and pathological tremors

“…Physiological tremor is a normal [8][9][10][11][12] Hz oscillatory movement of the outstretched hands, which occurs during maintained posture and to a lesser extent during movement execution. It can be accentuated by stress or fatigue and the dramatic increase in the tremor amplitude, which follows fear has been known from biblical times*.…”