The cerebellar cortex has a fundamental parasagittal organization that is apparent in the physiological response properties of Purkinje cells (PCs) and the expression of several molecular markers such as zebrin II (ZII). ZII is heterogeneously expressed in PCs such that there are sagittal stripes of high expression [ZII immunopositive (ZII+)] interdigitated with stripes of little or no expression [ZII immunonegative (ZII−)]. Several studies in rodents have suggested that climbing fiber (CF) afferents from an individual subnucleus in the inferior olive project to either ZII+ or ZII− stripes but not both. In this report, we show that this is not the case in the pigeon flocculus. The flocculus (the lateral half of folia IXcd and X) receives visual-optokinetic information and is important for generating compensatory eye movements to facilitate gaze stabilization. Previous electrophysiological studies from our lab have shown that the pigeon flocculus consists of four parasagittal zones: 0, 1, 2, and 3. PC complex spike activity (CSA), which reflects CF input, in zones 0 and 2 responds best to rotational optokinetic stimuli about the vertical axis (VA zones), whereas CSA in zones 1 and 3 responds best to rotational optokinetic stimuli about the horizontal axis (HA zones). In addition, folium IXcd consists of seven pairs of ZII+/− stripes. Here, we recorded CSA of floccular PCs to optokinetic stimuli, marked recording locations, and subsequently visualized ZII expression in the flocculus. VA neurons were localized to the P4+/− and P6+/− stripes and HA neurons were localized to the P5+/− and P7− stripes. This is the first study showing that a series of adjacent ZII+/− stripes are tied to specific physiological functions as measured in the responses of PCs to natural stimulation. Moreover, this study shows that the functional zone in the pigeon flocculus spans a ZII+/− stripe pair, which is contrary to the scheme proposed from rodent research.

The generation of compensatory eye movements in response to rotational head movements involves the transformation of visual-optokinetic and vestibular signals into commands controlling the appropriate eye muscles. Previously, it has been shown that the three systems (optokinetic, vestibular, and eye muscle) share a similar three-dimensional reference frame. In this report, we suggest that a peculiarity in the structure of the horizontal recti in pigeons demonstrates that the optokinetic system is organized with respect to the eye muscles rather than the vestibular canals. Measurements of the orientation of the plane for each of the lateral and medial recti were obtained. These were compared with the direction preferences of optokinetic neurons responsive to horizontal motion, namely “back” units in the nucleus of the basal optic root (nBOR), “forward” units in the pretectal nucleus lentiformis mesencephali (LM), and “vertical axis” (VA) Purkinje cells in the flocculus. The average direction preference of LM neurons excited in response to forward (temporal to nasal) visual motion, and VA Purkinje cells in response to optokinetic motion in the ipsilateral visual field was approximately parallel to the visual horizontal. This corresponded to the orientation of the medial rectus, which was also approximately parallel to the visual horizontal. The average direction preference of nBOR neurons excited in response to backward (nasal to temporal) visual motion, and VA Purkinje cells in response to optokinetic motion in the contralateral visual field was approximately 20–30 deg down from the visual horizontal. The orientation of the lateral rectus was also approximately 20–30 deg down from the visual horizontal. These data suggest that the incoming optokinetic signals are organized with respect to the outgoing extraocular muscle commands.

The avian nucleus of the basal optic root (nBOR) is a visual structure involved in the optokinetic response. nBOR consists of several morphologically distinct cell types, and in the present study, we sought to determine if these different cell types had differential projections. Using retrograde tracers, we examined the morphology and distribution of nBOR neurons projecting to the vestibulocerebellum (VbC), inferior olive (IO), dorsal thalamus, the pretectal nucleus lentiformis mesencephali (LM), the contralateral nBOR, the oculomotor complex (OMC) and a group of structures along the midline of the mesencephalon. The retrogradely labeled neurons fell into two broad categories: large neurons, most of which were multipolar rather than fusiform and small neurons, which were either fusiform or multipolar. From injections into the IO, LM, contralateral nBOR, and structures along the midline-mesencephalon small nBOR neurons were labeled. Although there were no differences with respect to the size of the labeled neurons from these injections, there were some differences with the respect to the distribution of labeled neurons and the proportion of multipolar vs. fusiform neurons. From injections into the VbC, the large multipolar cells were labeled throughout nBOR. The only other cases in which these large neurons were labeled were contralateral OMC injections. To investigate if single neurons project to multiple targets we used paired injections of red and green fluorescent retrograde tracers into different targets. Double-labeled neurons were never observed indicating that nBOR neurons do not project to multiple targets. We conclude that individual nBOR neurons have unique projections, which may have differential roles in processing optic flow and controlling the optokinetic response.

Neurons sensitive to optic flow patterns have been recorded in the the olivo-vestibulocerebellar pathway and extrastriate visual cortical areas in vertebrates, and in the visual neuropile of invertebrates. The complex spike activity (CSA) of Purkinje cells in the vestibulocerebellum (VbC) responds best to patterns of optic flow that result from either self-rotation or self-translation. Previous studies have suggested that these neurons have a receptive-field (RF) structure that “approximates” the preferred optic flowfield with a “bipartite” organization. Contrasting this, studies in invertebrate species indicate that optic flow sensitive neurons are precisely tuned to their preferred flowfield, such that the local motion sensitivities and local preferred directions within their RFs precisely match the local motion in that region of the preferred flowfield. In this study, CSA in the VbC of pigeons was recorded in response to a set of complex computer-generated optic flow stimuli, similar to those used in previous studies of optic flow neurons in primate extrastriate visual cortex, to test whether the receptive field was of a precise or bipartite organization. We found that these RFs were not precisely tuned to optic flow patterns. Rather, we conclude that these neurons have a bipartite RF structure that approximates the preferred optic flowfield by pooling motion subunits of only a few different direction preferences.