Cerebellar cortical organization: a one-map hypothesis

Hawkes R (2009) Cerebellar cortical organization: a one-map hypothesis.

Cerebellar cortical organization: a one map hypothesis…

Previous studies of cerebropontine projections have found that small regions of cerebral cortex provide terminal fields distributed into multiple clusters within BPN that aggregate to form concentric lamellae and receive inputs from different cerebral cortical regions (; ; ; ). A lamellar-like organization has also been reported for pontocerebellar projections (). In general, these studies support the view that somatotopical relationships are preserved within the cerebropontine projection and that the fractured somatotopical map characteristic of cerebellar cortical granular layer receptive fields () arises mainly from MF axon collateralization. In contrast, others have emphasized the importance of the initial cerebropontine stage in generating the fragmentation of the cerebellar cortical body map (, ; ).

Cerebellar cortical organization: a one-map hypothesis.

Cerebellar cortical organization: A one-map hypothesis

The aim of the present investigation was to study the fine grain anatomical relationships between cerebellar cortical connectivity and zebrin immunocytochemistry to test the one-map hypothesis. The results in the rat focus on microcircuit connections of the C1 zone in the copula pyramidis (CP) because the general anatomy and physiology of this region has been described previously () and because of its likely importance in limb movement (). Here, we show that at the microcircuit level, cerebellar cortical inputs and outputs are closely related to zebrin bands. Such findings provide strong support for the one-map hypothesis and extend the concept to PC outputs.

Cerebellar cortical organization: A one-map hypothesis.

Red and green fluorescently tagged beads (Retrobeads; Lumafluor) were used as retrograde tracers and biotinylated dextran amine (BDA, D-1956, 10,000 MW or D-7135, 3000 MW; 10% solution in saline; Invitrogen) was used for anterograde labeling. After the electrophysiological mapping stage of the experiment (see above), Retrobeads (4–30 nl) were pressure injected from a micropipette (tip diameter ∼ 20 μm) with a Picopump PV820 (WPI) into the cerebellar cortex, generating a small but clearly visible deposit of fluorescent tracer material just below the cortical surface (D,E). The anterograde tracer was injected using the same parameters as the Retrobeads. In most cases, the injection site of Retrobeads and/or BDA was immediately subjacent to the location on the surface where the largest cerebellar responses were evoked by peripheral stimulation of a particular body part—that is, each injection was usually made into approximately the center of a specific somatotopically defined cortical region within the C1 zone (hereafter termed “region”). Seven animals received a single Retrobeads injection, and nine animals received an injection of red Retrobeads into one cortical region and an injection of green Retrobeads into another, thereby generating a total of 25 Retrobead cases (for details, see , ). In the majority of these cases, BDA was also injected into the cortical location marked by a visible spot of Retrobeads (termed a paired injection site, n = 14; D–F). In the 14 animals that received paired Retrobead and BDA tracer injections, six animals received one or more additional injections of BDA into an additional cortical region. A further eight animals received either a single or two separate injections solely of BDA, thereby generating a total of 29 BDA cases. Five of these experiments used cerebellar surface anatomical landmarks to guide the placement of injections into the cerebellar cortex. All injection sites were made at a depth of approximately 0.2–0.3 mm perpendicular to the pial surface of the cerebellum.

HawkesCerebellar cortical organization: a one-map hypothesis.


cortical organization: a one-map hypothesis

The experiments detailed above using tracer injections into the cerebellar cortex provide evidence for a microcircuit organization within the input–output connectivity of the C1 zone in CP associated with the zebrin phenotype of PCs. If this relationship is genuine, then it would be expected that injections of retrograde tracer into restricted territories within AIN should result in labeling of PCs confined to individual zebrin bands within CP. This was tested in five additional experiments in which a retrograde tracer injection (∼2 nl) was targeted within medial AIN. In one of these experiments (Case #590; ), two (red and green) Retrobeads injections were both localized to different parts of medial AIN (A–C). Based on the cortical tracer results, the red injection site was centered on the termination area associated with zebrin band e1+, whereas the injection of green Retrobeads was centered on a more central area of AIN associated with zebrin band e1−.

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The one-map hypothesis postulates that, during embryogenesis, MFs and CFs use longitudinally oriented bands of PC clusters as a scaffold to organize their topography (). This leads to two predictions: (1) at the microcircuit level, there is an alignment between MF and CF terminations, and (2) that these terminations respect PC molecular marker boundaries. The results strongly support this hypothesis because they satisfy both of these predictions. The present study also extends the one-map concept by showing that this microcircuit connectivity is conserved in the pattern of PC outputs to the cerebellar nuclei.

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These competing viewpoints can be resolved by suggesting a two-step process in the transformation from an ordered cerebral map to a fractured cerebellar map. In the present study, when pontine cell labeling was pooled (thereby representing a significant fraction of the whole mediolateral width of the C1 zone in CP), most of the territory within BPN was occupied by labeled cells, forming a lamellar-like distribution. However, when cases were considered individually in relation to specific zebrin bands (and therefore at the level of individual microcircuits within the broader C1 zone), the cell labeling generally formed multiple clusters within BPN. In double tracer studies in which the two injection sites were centered on different zebrin bands, the clusters of pontine cell labeling were mainly non-overlapping. Therefore, at the level of a whole cerebellar zone, a lamellar organization is present within BPN, but the spatial distribution fragments into multiple cell clusters at a microcircuit level of resolution.