Inferior olivary projection to the zebrin II stripes in lobule IXcd of the pigeon flocculus: A retrograde tracing study

Abstract

Zebrin II (ZII; a.k.a. aldolase C) is expressed heterogeneously in Purkinje cells (PCs) such that there are sagittal stripes of high expression (ZII+) interdigitated with stripes of little or no expression (ZII-). The pigeon flocculus receives visual-optokinetic information and is important for generating compensatory eye movements. It consists of 4 sagittal zones based on PC complex spike activity (CSA) in response to rotational optokinetic stimuli. There are two zones where CSA responds best to rotation about the vertical axis (VA), interdigitated with two zones where CSA responds best to rotation about an horizontal axis (HA). These optokinetic zones relate to the ZII stripes in folium IXcd of the flocculus, such that an optokinetic zone spans a ZII+/- pair: the HA zones span the P5+/- and P7+/- ZII stripe pairs, whereas the VA zones correspond to ZII stripe pairs P4+/- and P6+/-. In the present study, we used fluorescent retrograde tracing to determine the olivary inputs to the ZII+ and ZII- stripes within the functional pairs. We found that separate but adjacent areas of the medial column of the inferior olive (mcIO) project to the ZII+ and ZII- stripes within each of the functional pairs. Thus, although a ZII+/- stripe pair represents a functional unit in the pigeon flocculus insofar as the CSA of all PCs in the stripe pair encodes similar sensory information, the olivary inputs to the ZII+ and ZII- stripes arise from different, although adjacent, regions of the mcIO.

Cerebellar Modules and Their Role as Operational Cerebellar Processing Units

“…We have shown that they receive CF input from separate, but adjacent areas of the mcIO (Fig. 4 c) [ 81 , 82 ], and there is some suggestion that the ZII+ and ZII− PCs have differential projections [ 76 ]. We have some evidence that the CSA of ZII+ PCs shows a greater depth of modulation to optic flow stimuli, compared to the ZII− PCs within the same functional unit [ 83 ].…”

“…Best-known examples of the functional properties of cerebellar modules are illustrated by the ample bulk of research studying the adaptive control of reflexive eye and head movements. Here, individual floccular modules control movements around a particular visual axis [ 82 , 236 , 237 ]. However, it should be noted that also in the vestibulocerebellum, several non-adjacent zones seem to be present with basically the same function [ 71 ].…”

Topographic Organization of Inferior Olive Projections to the Zebrin II Stripes in the Pigeon Cerebellar Uvula

“…Finally, lateral to this and spanning the lateral half of P2+ (P2+lat) and the P2− stripe, is a zone containing neurons responsive to optic flow resulting from “descent”. Previously we have shown that the inputs to the ZII+ and ZII− stipes in the flocculus (i.e., stripes P4+/− to P6+/−) receive CF input from separate, but adjacent areas of the inferior olive (IO; Wylie et al, 2017 ). The ZII+ stipes within the VA zones (P4+ and P6+) receive input from the caudal-most portion of the mcIO while the ZII− stripes of the VA zones (P4− and P6−) are innervated by a slightly more rostral region of the mcIO.…”

“…In the pigeon vestibulocerebellum (VbC), we have shown that the ZII stripes coincide with functional properties of PCs and afferent inputs (Pakan and Wylie, 2008 ; Pakan et al, 2010 , 2011 , 2014 ; Graham and Wylie, 2012 ; Wylie et al, 2013 , 2017 ). The avian VbC, which consists of folia IXcd and X, contains PCs whose complex spike activity (CSA) are responsive to optic flow patterns resulting from self-motion (Wylie and Frost, 1991 ).…”

“…The ZII+ stipes within the VA zones (P4+ and P6+) receive input from the caudal-most portion of the mcIO while the ZII− stripes of the VA zones (P4− and P6−) are innervated by a slightly more rostral region of the mcIO. Similarly, the ZII+ stripes of the HA zones are innervated by a more caudal region of the mcIO than the ZII− stripes of the HA zone, which are innervated by the rostral-most mcIO (Wylie et al, 2017 ). Thus, although a ZII+/− stripe pair represents a functional unit in the flocculus whereby all PCs respond to the same pattern of optic flow (either VA or HA), the ZII+ and ZII− stripes receive optic flow from different areas of the IO.…”