Cerebellar cortical activity in the cat anterior lobe during hindlimb stepping

Abstract

We recorded from over 250 single cortical neurons throughout the medial anterior lobe of the cat cerebellum during passive movements of the ipsilateral hindlimb resembling stepping on a moving treadmill. We applied three different quantitative analysis techniques to determine the extent of neuronal modulation that could be accounted for by the stepping movements. The analyses all indicated that up to half the recorded neurons in all five lobules responded to these passive hindlimb movements. We reconstructed the locations of the recorded neurons on a 2-D map of the cerebellar cortex in order to determine the spatial distribution of responsive cells. Cells that were located in the classical hindlimb projection areas of the anterior lobe (in lobules 2 and 3) were generally most responsive to the limb movement with activity patterns that generally had a linear relationship to hindlimb kinematics. Cells in lobules 4 and 5, considered as classical forelimb areas of the cerebellum, were also responsive. Although these cells tended to have noisier firing patterns, many were found to be modulated nevertheless by the hindlimb movements. We also found a clear demarcation between zones b and c, with a higher fraction of responsive cells in all lobules located in zone b.

Reevaluation of the Beam and Radial Hypotheses of Parallel Fiber Action in the Cerebellar Cortex

“…Both direct activation of CF afferents (presynaptic component) and antidromic activation of PCs likely contribute to the remaining response. Indeed, the center response has a parasagittal shape consistent with the projection pattern of the CF afferents (Sasaki et al, 1989;Chen et al, 1996). To quantify the geometry of the response evoked by WM stimulation, we measured the length of the response along the ML and RC axes of the folium and determined the ratio of the ML/RC axes.…”

“…In support of this hypothesis, MF input evokes field potentials in the molecular layer well outside of the MF termination area (Garwicz and Andersson, 1992), whisker stimulation comodulates transversely located PCs (Bosman et al, 2010), and the presence of synchrony in the simple spike firing during natural inputs (De Zeeuw et al, 1997). However, the beam hypothesis is controversial as others reported that peripheral or MF inputs evoke only patches of PC or molecular layer activity (Bower and Woolston, 1983;Cohen and Yarom, 1998;Rokni et al, 2007;Santamaria et al, 2007). Others found little temporal synchrony in the simple spike discharge of PCs separated transversely by Ͼ100 m (Bell and Grimm, 1969;Ebner and Bloedel, 1981;Shin and De Schutter, 2006;Heck et al, 2007).…”

“…The alternative hypothesis is based on the radial organization of GC axons as they ascend to the molecular layer and make synaptic contacts on PCs (Llinas, 1982;Napper and Harvey, 1988;Gundappa-Sulur et al, 1999;Santamaria et al, 2002;Santamaria and Bower, 2005;Lu et al, 2009). This "radial" hypothesis postulates that GC ascending axons provide the dominant input to PCs and that PCs located laterally are very weakly activated by PFs.…”

“…Compared with PF synapses, the synaptic connections made along the ascending limb are argued to be stronger, have a higher number of connections on a PC, and result in more synchronous activation of PCs (Llinas, 1982;Isope and Barbour, 2002;Sims and Hartell, 2005). Modeling studies found little role for PFs in modulating PC simple spike discharge, suggesting instead PFs provide background tone (Santamaria and Bower, 2005;Santamaria et al, 2007).…”

“…In the cerebellar slice, synaptic strength between ascending GC axons and PCs, and between PFs and PCs is equivalent, and PFs activate PCs for several hundred microns (Isope and Barbour, 2002;Walter and Khodakhah, 2009). A variant of the radial hypothesis proposes that GABAergic, molecular layer inhibition prevents beam-like activation by PFs (Santamaria et al, 2002(Santamaria et al, , 2007.…”