Receptive Fields Of Neurons In Superior Colliculus Influenced By Association Cortices And Sensory Cue Of Different Modality

Superior colliculus (SC) is an important structure of the brain and plays an important role in the orientation movement of the head and eyes. The deep layer of SC receives multiple sensory inputs from a wide range of cortical and subcortical sources, which makes the deep layer of SC rich of multisensory neurons. Each sense forms a complete topographic map of spatial receptive fields. Thus, neurons located in different areas of SC are able to sense the stimuli in different place of the external environment. For a typical SC multisensory neuron, their spatial receptive fields (RFs) of different senses are well overlapped spatially, which is important for them to integrate multisensory inputs effectively. However, we don’t know how this property of SC neuron is formed, and whether it relies on high-order cortices. Similarly, we are unclear about how different sensory inputs interact with each other and whether RFs of multisensory neurons can change with different contexts dynamically? Using the single-neuron electrophysiological recording and the reversible cortical deactivation of cryogenic cooling, we try to explore these issues in cats.In the first part of our study, we recorded a total of 157 visual-auditory multisensory neurons in the cat SC. We recorded and analyzed their responsiveness to sequential presentation of multisensory stimuli (visual stimulus preceding by auditory stimulus or the reverse), in which the spatial location of first stimulus is fixed, the second stimulus varied with their spatial positions from -900～900 (stepped by 150) in azimuth and the time interval between stimuli was set to just separate evoked responses. The results demonstrated that the presentation of the preceding stimulus could dramatically shift the spatially location of RF isolated by the second stimulus in most cases, suggesting that different sensory inputs interacted with each other. RFs could shift bilaterally (laterally or medially) and is not sensory-specific although visual RFs shifted a bit more. Further tests showed that, the magnitude of RF shift was relied to the spatial location and the intensity of the first stimulus as well as the SO A (stimulus onset asynchrony). Usually, the RF would shift more if the spatial location of the first stimulus was a bit far away from the RF centers, or if the stimulus of the strong intensity was used and the short SOA was applied.In the second part, we studied the influence of the association cortices (AES) on RFs in superior colliculus (SC) neurons. A total of 114 visual-auditory multisensory neurons recorded in the cat SC were examined. The results demonstrated that deactivation of one of associated cortices could dislocate the visual and auditory spatial receptive fields (RFs) and shrank their size, which resulted in the separation between visual and auditory RFs. Further analysis demonstrated that this RF separation significantly correlated with the decrement of neurons’ multisensory enhancement (ME). In addition, the stimulus effectiveness greatly influenced the effect of cortical deactivation, with the more separation of RFs in the condition of low stimulus intensity. To further test the conclusion stated above, the effect of changing RF size by modulating stimulus intensities on neurons’ multisensory integration was examined in 35 neurons. When cortices were deactivated, mean ME across populations decreased in each level of stimulus intensity but more in the low effective condition and less in the higher effective conditions. These results revealed the new neural mechanism underlying high-order cortices modifying activities of SC.Our results indicated that sensory inputs of different modalities have complex interactions with each other and different brain regions work together to be involved in the process of multisensory integration, which enriched our understanding of the multisensory process of the brain, and provided the neural mechanism for how the brain dynamically integrate multisensory cues in different contexts. SC and association cortices are the critical parts of the motor neural circuits, and the damage of them (even just partly) could seriously affect the sensory and motor function of people or animals. Thus, our research results also can provide pathological diagnosis knowledge for the functional decline of multisensory and/or sensory-motor integrations, caused by the external force trauma, stroke, all kinds of diseases, etc.