Correlations Between Purkinje Cell Single-Unit Activity and Simultaneously Recorded Field Potentials in the Immediately Underlying Granule Cell Layer

Abstract

Lu, Huo, Mitra J. Hartmann, and James M. Bower. Correlations between Purkinje cell single-unit activity and simultaneously recorded field potentials in the immediately underlying granule cell layer. J Neurophysiol 94: 1849 -1860, 2005. First published May 31, 2005 doi:10.1152/jn.01275.2004. Evidence from both anatomical and physiological studies suggests that the ascending segment of the granule cell axon provides a large, driving input to overlying Purkinje cells. In the current experiments, we used dual recording electrodes to simultaneously record spike activity of Purkinje cells and multiunit field potential activity in the directly underlying granule cell layer. These dual recordings were performed both during periods of spontaneous ("background") firing and also after peripheral tactile stimulation. The results demonstrate that in the large majority of cases, there is a strong positive correlation between spontaneous Purkinje cell simple spikes and spontaneous activity in the immediately underlying granule cell layer. The strength of this correlation was dependent on both the firing rate of the Purkinje cell as well as on the rate of granule cell layer multiunit activity. In addition, for any given pair of recordings, the correlation seen during spontaneous activity accurately predicted the magnitude and time course of responses evoked by peripheral tactile stimulation. These results provide additional evidence that the synapses associated with the ascending segment of the granule cell axon have a substantial influence on Purkinje cell output. This relationship is considered in the context of our ongoing reevaluation of the physiological relationship between cerebellar granule and Purkinje cells. I N T R O D U C T I O NThe unusual and geometrically stereotyped relationship between the parallel fiber axonal system and the Purkinje cells (PCs) has strongly influenced cerebellar theories for more than 50 years (Albus

Tactile Stimulation Evokes Long-Term Synaptic Plasticity in the Granular Layer of Cerebellum

“…T and C corresponded to the trigeminal and cortical responses previously observed in Crus-IIa (Bower and Woolston, 1983;Morissette and Bower, 1996) (L. Roggeri and E. D'Angelo, unpublished observations). The D (delayed) wave was not reported previously [but see Lu et al (2005), their Fig. 7] and may correspond to signals elaborated in brainstem circuits (Kleinfeld et al, 1999;O'Connor et al, 2002).…”

“…The exposure of the cerebellar surface was performed following surgical procedures reported previously (Bower and Woolston, 1983;Morissette and Bower, 1996;Lu et al, 2005). Briefly, after the skin and muscles were dislocated (during this phase, cutaneous reflexes were reduced with 0.2 ml of lidocaine; AstraZeneca) and the bone was cleaned, a 0.5 mm hole was drilled 2-3 mm posterior and 3-4 mm lateral from lambda on the left hemisphere to expose the cerebellar surface in correspondence to Crus-IIa.…”

Topography and Response Timing of Intact Cerebellum Stained With Absorbance Voltage-Sensitive Dye

“…Axons from granule cells ascend to the ML synapse with PCs during the ascent and bifurcate to form parallel fibers (Huang et al 2006;Tolbert et al 2004). Stimulating mossy fibers activates a local patch of PCs via ascending axons of granule cells (Bower and Devor 2003;Cohen and Yarom 1998;Rokni et al 2007), as shown by correlated activity of granule cells and their overlying PCs (Lu et al 2005). Similar patches of Cb activation were observed during tactile stimulation (Bower and Woolston 1983) in intact rats.…”

The Spatial Organization of Long-Term Synaptic Plasticity at the Input Stage of Cerebellum

“…In the LTP channel, the delay is reduced and the average frequency of granule cell discharge is enhanced, whereas the opposite happens in the LTD channel (Nieus et al, 2006). By doing so, the LTP (or LTD) channels could favor (or prevent) the activation of specific Purkinje cell and molecular layer interneuron assemblies (Bower, 2002;Lu et al, 2005) as well as the development of short-term (Isope and Barbour, 2002;Sims and Hartell, 2005) and long-term synaptic plasticity (Hansel et al, 2001;Casado et al, 2002) at the corresponding parallel fiber synapses.…”