Characterization of motor functions of the human Superior Colliculus using fMRI

Abstract

The Superior Colliculus (SC) is well established to be a structure that plays a major role in orienting the eyes and head towards objects of interest in the surroundings. Most of the studies in the SC thus far have been conducted on non-human primates. Although the neural architecture is presumed to be similar, existence of differences in anatomy, afferents and efferents between the SC of different mammals questions functional extrapolation of such studies to humans. Also, there have been very few electrophysiological studies that have investigated the role of the SC in reaching and finger tapping movements. An fMRI study in humans conducted earlier in the lab was the first to show that the SC is involved in reaching movements in humans. In order to further elucidate the motor functions of the SC in humans, we conducted three experiments and analysed one pre-acquired dataset. These studies used two simple and classical paradigms – reaching, and finger tapping movements. The SC is widely believed to be a visually driven structure, supported by numerous studies in macaques. With our first study, we sought to decipher if the SC is also active in response to reaching, guided by tactile stimulation. We designed a task where subjects had to maintain fixation while performing reaching movements to peripheral targets that were either visual or tactile in nature, separated by their respective blocks. We found that the SC indeed shows activity in response to somatically or visually guided reaching, but not to visual stimulation or somatic stimulation on their own. In addition, we also observed a strong signal contribution from button presses in tasks with control conditions, which were required to be performed by subjects in response to oddball stimuli, to make sure that they were engaged in the tasks. Our second study was divided into two parts. The first part consisted of an analysis of the finger tapping task (motor task section) from the Human Connectome Project (HCP) database. The second part of the study investigated whether complex finger tapping and simple finger tapping movements, paced by visual or auditory stimuli, caused an activation in the SC. We found no activation in response to the finger tapping task from the HCP data. We also found that the SC did not take part in either the complex or simple finger tapping tasks that we conducted. This, together with the results corresponding to finger tapping from the HCP data, and the finger tapping (recorded as button presses) results from the first experiment, led us to postulate that the SC might be involved only when finger tapping movements occur in response to novel stimuli. With our third and final study, we investigated the response of the SC to novel stimuli. In the experiment, subjects responded with button presses or counting to oddballs involving the same modalities as the first experiment: visual and somatic stimulation. We found some activity in response to all oddball conditions combined together. This activity was further weakened when oddballs were bifurcated into four conditions by the sensory modalities involved - visual and somatic stimulation and the corresponding responses - button presses and counting. Although these results hint that the SC might respond to oddball stimulation, these effects were not consistent across subjects warranting further investigation for more concrete conclusions. Taken together, our results conclusively show that apart from visual information the SC integrates sensory information such as touch towards the execution of reaching movements. In addition, the SC does not play a role in the execution of movement sequences that are repetitive, irrespective of whether they are complex or simple movements. For a concrete conclusion regarding responses to novel stimuli, more sensitive experiments are necessary.