Characteristics of Responses of Golgi Cells and Mossy Fibers to Eye Saccades and Saccadic Adaptation Recorded from the Posterior Vermis of the Cerebellum

Abstract

The anatomical organization of the granular layer of the cerebellum suggests an important function for Golgi cells (GC) in the pathway conveying mossy fiber (MF) afferents to Purkinje cells. Based on such anatomic observations, early proposals have attributed a role in "gain control" for GCs, a function disputed by recent investigations, which assert that GCs instead contribute to oscillatory mechanisms. However, conclusive physiological evidence based on studies of cerebellum-dependent behavior supporting/dismissing the gain control proposition has been lacking as of yet. We addressed the possible function of this interneuron by recording the activity of a large number of both MFs and GCs during saccadic eye movements from the same cortical area of the monkey cerebellum, namely the oculomotor vermis (OMV). Our cellular identification conformed to previously established criteria, mainly to juxtacellular labeling studies correlating physiological parameters with cell morphology. Response patterns of both MFs and GCs were highly heterogeneous. MF discharges correlated linearly with eye saccade metrics and timing, showing directional preference and precise direction tuning. In contrast, GC discharges did not correlate strongly with the metrics or direction of movement. Their discharge properties were also unaffected by motor learning during saccadic adaptation. The OMV therefore receives a barrage of information about eye movements from different oculomotor areas over the MF pathway, which is not reflected in GCs. The unspecificity of GCs has important implications for the intricacies of neuronal processing in the granular layer, clearly discrediting their involvement in gain control and instead suggesting a more secluded role for these interneurons.

Spontaneous Activity Signatures of Morphologically Identified Interneurons in the Vestibulocerebellum

“…Therefore, the high, very regular frequencies seen in granular layer recordings of the flocculus of the awake monkey (Miles et al, 1980) may not have reflected Golgi cells, but rather UB cells, whose extensive presence in the flocculus was not known at that time. Cells whose ISI histograms are like those of Golgi cells identified in the present study have been found in the vermis of the awake monkey (Prsa et al, 2009). Recent observations in slices showed that Golgi cells possess conductances enabling autorhythmicity.…”

Current source density correlates of cerebellar Golgi and Purkinje cell responses to tactile input

“…A vertical organization of mossy-fiber input to the granular layer has recently been reported in the decerebrate cat (Jörntell and Ekerot 2006). Whereas in the latter study this resulted in modality-specific responses of granule cells, the present study and previous ones (Holtzman et al 2006;Prsa et al 2009;Vos et al 2000) indicate that GoCs integrate synaptic input from multiple receptive fields. A layered projection pattern could result from the layered distribution of attractants or repellants (Solowska et al 2002).…”

“…For the responses studied here, the broad activation (Fig. 10) implies a considerable convergence of mossy fibers onto GoCs and a loss of GoC selectivity (Prsa et al 2009). Whereas the lack of a trigeminal or putatively corticopontine peak in some GoCs, or equivalently in the same GoC at particular stimulus positions, may be explained as a selectivity in the mossy-fiber projection pattern, this would imply as well that the trigeminal and pontine projections are not perfectly aligned.…”

“…In addition, both the initial burst-like response and the long-lasting suppression could reflect the activation of afferent synapses or, alternatively, be generated by intrinsic membrane mechanisms (Solinas et al 2007). Moreover, despite their stereotypical response patterns to peripheral stimulation, GoCs have larger receptive fields and a lower response selectivity than mossy fibers (Prsa et al 2009). This loss of specificity was attributed to their presumed wide input via parallel fibers Vos et al 2000).…”

Pseudobulbar affect: the spectrum of clinical presentations, etiologies and treatments

“…Although these speculations are intriguing because of the use of serotonergic and antiglutamatergic drugs in PBA, the function of various cells and neurotransmitters within the cerebellar microcircuitry, or their specific role in PBA, has not been clearly defined, and researchers continue their efforts to elucidate potential mechanisms within this circuitry and their potential role in cerebro-cerebellar loops [50][51][52][53].…”