Abstract:
Arguably visual information is the most important source of sensory information for us human beings, allowing us to perceive the world. Almost a quarter of our brain is devoted to visual processing. To achieve a precise projection of objects of interest onto the retinal fovea, the region offering the highest spatial resolution and other advantages for the analysis of visual objects, two major types of eye movements, saccades and smooth pursuit are deployed. Saccades shift the image of an object of interest into the fovea. In case the object should be moving, smooth pursuit eye movements (SPEM) try to keep the image of the object within the confines of the fovea in order to ensure sufficient time for its analysis.
It has been known that the oculomotor vermis (OMV) of the cerebellar cortex is dedicated to the control of both saccades and SPEM. However, it has remained unclear if the same oculomotor vermal neurons contribute to controlling these two different types of movements, a scenario that does not look very likely considering their dramatically different kinematics. To address this question, we recorded the activity of OMV Purkinje cells (PCs), the only type of output neuron of cerebellar cortex, in monkeys, and the most suitable animal model for studies of the cerebellar control of eye movements made by humans. During recordings the monkeys were performing saccades and smooth pursuit eye movement (SPEM). Subjecting the recorded saccade and SPEM related PC simple spike responses to a multiple regression analysis, we found that, for saccades, the neural firing pattern is mainly determined by eye position. In contrast, in the case of SPEM, eye velocity plays the most important role in defining the firing pattern. These results indicate that the cerebellar computations for saccades and SPEM are different, even at the level of individual PCs.
Both saccades and SPEM can be adaptively changed by the experience of insufficiencies, compromising the precision of saccades or the minimization of object image slip in the case of SPEM. As both forms of adaptation rely on the cerebellar oculomotor vermis (OMV), most probably deploying a shared neuronal machinery, one might expect that the adaptation of one type of eye movement should affect the kinematics of the other. In order to test this expectation, we subjected 2 monkeys to a standard saccadic adaption paradigm with SPEM test trials at the end and, alternatively, the same 2 monkeys plus a 3rd one to a random saccadic adaptation paradigm with interleaved trials of SPEM. In contrast to our expectation we observed at best marginal transfer which, moreover was little consistent across experiments and subjects. The lack of consistent transfer of saccadic adaptation decisively constrains models of the implementation of oculomotor learning in the OMV, suggesting an extensive separation of saccade and SPEM-related synapses on P-cell dendritic trees.
The OMV projects ipsilaterally to the caudal fastigial nuclei (cFN) (Yamada & Noda, 1987), which is also called the fastigial oculomotor region. Not surprisingly, in view of the established role of the OMV in the control of saccades and SPEM, also the cFN is known to contribute to both.
Microsaccades are small saccades produced during fixation, whose amplitudes are <1 degree. The concept of a microsaccade-saccade continuum is supported by the fact that studies on the underpinnings of microsaccades have shown that those oculomotor structures explored contribute to saccades of all sizes. The OMV is one of these structures for which a microsaccade-macrosaccade continuum has been established. As shown in this second work package, this continuum is maintained at the level of the cFN, the recipient of saccade-related signals from the OMV. Furthermore, we demonstrate that the pre-microsaccadic baseline firing rate of cFN neurons has properties suitable to ensure precise fixation.
In summary, our results demonstrate the participation of the cerebellum in the control of saccades and SPEM at the level of cerebellar cortex as well as at the level of the caudal fastigial nucleus. It establishes that, contrary to the still dominating view of a separation of the cerebellar machinery for saccades and SPEM, these two forms of goal-directed eye movements rely on largely overlapping, if not identical circuitry. Irrespective of this overlap, learning based adjustments maintain a stunning degree of independence. This is established by our behavioral work. It suggests that this specificity may be a consequence of delimiting distinct dendritic territories of OMV Purkinje cells for the two types of eye movements. Finally, this work supports the notion of a general micro- macrosaccade continuum by establishing that also cFN neurons care for both, micro- and macrosaccades.
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