Topography of visual and somatosensory inputs to the pontine nuclei in zebra finches (Taeniopygia guttata).

Birds have a comprehensive network of sensorimotor projections extending from the forebrain and midbrain to the cerebellum via the pontine nuclei, but the organization of these circuits in the pons is not thoroughly described. Inputs to the pontine nuclei include two retinorecipient areas, nucleus lentiformis mesencephali (LM) and nucleus of the basal optic root (nBOR), which are important structures for analyzing optic flow. Other crucial regions for visuomotor control include the retinorecipient ventral lateral geniculate nucleus (GLv), and optic tectum (TeO). These visual areas, together with the somatosensory area of the anterior (rostral) Wulst, which is homologous to the primary somatosensory cortex in mammals, project to the medial and lateral pontine nuclei (PM, PL). In this study, we used injections of fluorescent tracers to study the organization of these visual and somatosensory inputs to the pontine nuclei in zebra finches. We found a topographic organization of inputs to PM and PL. The PM has a lateral subdivision that predominantly receives projections from the ipsilateral anterior Wulst. The medial PM receives bands of inputs from the ipsilateral GLv and the nucleus laminaris precommisulis, located medial to LM. We also found that the lateral PL receives a strong ipsilateral projection from TeO, while the medial PL and region between the PM and PL receive less prominent projections from nBOR, bilaterally. We discuss these results in the context of the organization of pontine inputs to the cerebellum and possible functional implications of diverse somato-motor and visuomotor inputs and parcellation in the pontine nuclei.

Topography of optic flow processing in olivo-cerebellar pathways in zebra finches (Taeniopygia guttata).

In birds, the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali (LM) are brainstem nuclei involved in the analysis of optic flow. A major projection site of both nBOR and LM is the medial column of the inferior olive (IO), which provides climbing fibers to the vestibulocerebellum. This pathway has been well documented in pigeons, but not other birds. Recent works have highlighted that zebra finches show specializations with respect to optic flow processing, which may be reflected in the organization of optic flow pathways to the IO. In this study, we characterized the organization of these pathways in zebra finches. We found that the medial column consists of at least eight subnuclei (i-viii) visible in Nissl-stained tissue. Using anterograde traces we found that the projections from LM and nBOR to the IO were bilateral, but heavier to the ipsilateral side, and showed a complementary pattern: LM projected to subnucleus i, whereas nBOR projected to subnuclei ii and v. Using retrograde tracers, we found that these subnuclei (i, ii and v) projected to the vestibulocerebellum (folia IXcd and X), whereas the other subnuclei projected to IXab and the lateral margin of VII and VIII. The nBOR also projected ipsilaterally to the caudo-medial dorsal lamella of the IO, which the retrograde experiments showed as projecting to the medial margin of VII and VIII. We compare these results with previous studies in other avian species.

Cerebellar Inputs in the American Alligator (Alligator mississippiensis).

Crocodilians (alligators, crocodiles, and gharials) are the closet living relatives to birds and, as such, represent a key clade to understand the evolution of the avian brain. However, many aspects of crocodilian neurobiology remain unknown. In this paper, we address an important knowledge gap as there are no published studies of cerebellar connections in any crocodilian species. We used injections of retrograde tracers into the cerebellum of the American alligator (Alligator mississippiensis) to describe for the first time the origin of climbing and mossy fiber inputs. We found that inputs to the cerebellum in the American alligator are similar to those of other nonavian reptiles and birds. Retrograde labeled cells were found in the spinal cord, inferior olive, reticular formation, vestibular and cerebellar nuclei, as well as in nucleus ruber and surrounding tegmentum. Additionally, we found no retrogradely labeled cells in the anterior rhombencephalon which suggest that, like other nonavian reptiles, crocodilians may lack pontine nuclei. Similar to birds and other nonavian reptiles, we found inputs to the cerebellum from the pretectal nucleus lentiformis mesencephali. Additionally, we found retrogradely labeled neurons in two nuclei in the pretectum: the nucleus circularis and the interstitial nucleus of the posterior commissure. These pretectal projections have not been described in any other nonavian reptile to date, but they do resemble projections from the nucleus spiriformis medialis of birds. Our results show that many inputs to the cerebellum are highly conserved among sauropsids and that extensive pretectal inputs to the cerebellum are not exclusive to the avian brain. Finally, we suggest that the pontine nuclei of birds are an evolutionary novelty that may have evolved after the last common ancestor between birds and crocodilians, and may represent an intriguing case of convergent evolution with mammals.

Pretecto- and ponto-cerebellar pathways to the pigeon oculomotor cerebellum follow a zonal organization.

Both birds and mammals have relatively large forebrains and cerebella. In mammals, there are extensive sensory-motor projections to the cerebellum through the pontine nuclei originating from several parts of the cerebral cortex. Similar forebrain-to-cerebellum pathways exist in birds, but the organization of this circuitry has not been studied extensively. Birds have two nuclei at the base of the brainstem that are thought to be homologous to the pontine nuclei of mammals, the medial and lateral pontine nuclei (PM, PL). Additionally, birds are unique in that they have a pretectal nucleus called the medial spiriform nucleus (SpM) that, like the pontine nuclei, also receives projections from the forebrain and projects to the oculomotor cerebellum (OCb; folia VI to VIII). The OCb also receives input from the pretectal nucleus lentiformis mesencephali (LM), which analyzes visual optic flow information resulting from self-movement. In this study, we used single or double injections of fluorescent tracers to study the organization of these inputs from PM, PL, SpM and LM to the OCb in pigeons. We found that these inputs follow a zonal organization. The most medial zone in the OCb, zone A1, receives bilateral inputs from the lateral SpM, PL and LM. Zones A2 and C receive a bilateral projection from the medial SpM, and a mostly contralateral projection from PM and LM. We discuss how the pathway to zone A1 processes mainly visuo-motor information to spinal premotor areas, whereas the pathways to zone A2/C processes somato-motor and visuo-motor information and may have a feedback/modulatory role.