Compartmentalization of the chick cerebellar cortex based on the link between the striped expression pattern of aldolase C and the topographic olivocerebellar projection

Abstract

The avian cerebellum is organized into multiple longitudinal stripes defined by expression profiles of aldolase C (zebrin II) in Purkinje cells. The relationship between the aldolase C striped pattern and the olivocerebellar projection pattern is crucial in understanding cerebellar functional compartmentalization. We identified all aldolase C stripes across all lobules with the serial section alignment analysis method and then looked at this relationship by anterograde and retrograde labeling of olivocerebellar axons in the chick cerebellum. Aldolase C stripes were generally consistent and continuous from lobule I through VII and to the medial part of lobules VIII-IXb. The dorsal and ventral lamellas (DL, VL) of the inferior olive projected to the stripes in these areas with a simple mediolateral topographic relation. A few aldolase C stripes appeared at the lateral edge of lobules VI-VIII. Several more stripes were added in the lateral parts of lobules IXa-IXb and IXc-X. The medial column (MC) of the inferior olive projected to the stripes in lobules VIII-X, including the added lateral stripes, with a complex topographic relation. Sharp boundaries between aldolase C-positive and -negative stripes often accompanied a gap in the Purkinje cell layer and bordered topographically distinct groups of axons. Although the compartmental organization of the chick cerebellum is comparable to that of the mammalian cerebellum, several significant differences in the organization suggest partly separate evolutionary lineages of the mammalian and avian cerebella. We propose that rostral lobules may be evolved by rostral extension of medial stripes from caudal lobules in the avian cerebellum.

Is Cerebellar Architecture Shaped by Sensory Ecology in the New Zealand Kiwi <b><i>(Apteryx mantelli)</i></b><b>?</b>

“…Another interesting feature of folium IV is the sharp lateral border of stripe 3 as well as the gap in the Purkinje cell layer of this stripe ( fig. 8 b), which was also noted in chicken by Vibulyaseck et al [2015].…”

“…The architecture of the parasagittal stripes and transverse regions present in the kiwi cerebellum generally conforms to the pattern reported for many other avian and mammalian species [Ozol et al, 1999;Armstrong et al, 2000;Sillitoe et al, 2005;Pakan et al, 2007;Iwaniuk et al, 2009b;Marzban et al, 2010;Corfield et al, 2015;Vibulyaseck et al, 2015]. The kiwi cerebellum can be subdivided into an anterior region and a posterior region based on the presence of ZII+/-stripe pairs and also a central, nodular, and lingular region by uniform ZII+ expression.…”

“…A large central region has been attributed to gaining flight in bats [Kim et al, 2009], and therefore it is possible that the opposite has occurred in kiwi and tinamous; flightlessness has removed the extra motor and cognitive aspects needed for flight and has thus led to a reduced central region. However, this feature would also be expected in chickens, which is not the case [Marzban et al, 2010;Vibulyaseck et al, 2015]. Another factor that could influence the size/structure of the central zone is that it also receives acoustic and possibly trigeminal inputs [Snider and Stowell, 1944;Whitlock, 1952;Voogd and Barmack, 2006].…”

“…Although the mammalian and avian cerebella show some fundamental differences, research defining the corticonuclear and olivocerebellar connections of the Purkinje cell zones in both groups has allowed for detailed homologies between the mammalian and avian zonal patterns [Arends and Voogd, 1989;Arends and Zeigler, 1989;Sugihara and Shinoda, 2004;Vibulyaseck et al, 2015]. Therefore, information on the functional aspects of the mammalian zones can help shed some light on questions concerning the sensory ecology of the avian cerebellum.…”

“…In mammals, motor regions in the vermis of the cerebellum play a role in postural control and are engaged in locomotion [Voogd, 2016], whereas the more lateral regions of the hemispheres are involved in more distal movements, especially of the forelimbs [Horn et al, 2010]. In chickens, it has been shown that the 3-stripe is equivalent to the B-zone in the mammalian cerebellum and represents the boundary between the vermis and the hemisphere [Marzban et al, 2010;Vibulyaseck et al, 2015]. In kiwi, the boundary between stripes 3+ and 3-was sharp and 3+ usually had a gap in the Purkinje cell layer.…”