Abstract
The responses of neurons in the visual pathway depend on the context in which a stimulus is presented. Responses to predictable stimuli are usually suppressed, highlighting responses to unexpected stimuli that might be important for behaviour. Here we established how context modulates the response of neurons in the superior colliculus, a region important in orienting towards or away from visual stimuli. We made extracellular recordings from single-units in the superficial layers of superior colliculus in awake mice. We found strong suppression of visual response by spatial context (surround suppression) and temporal context (adaptation). Neurons showing stronger surround suppression also showed stronger adaptation effects. In neurons where it was present surround suppression was dynamic, and was reduced by adaptation. Adaptation’s effects further revealed two components to surround suppression: one component that was weakly tuned for orientation and adaptable, and another component that was more strongly tuned but less adaptable. The selectivity of the tuned component was flexible, such that suppression was stronger when the stimulus over the surround matched that over the receptive field. Our results therefore reveal strong interactions between spatial and temporal context in regulating the flow of signals through mouse superior colliculus, and suggest the presence of a subpopulation of neurons that might signal novelty in either space or time.
SIGNIFICANCE STATEMENT Our senses provide enormous amounts of information, and the central nervous system needs to filter this information to focus on potentially important objects. Here we study two visual mechanisms that might highlight unexpected or surprising objects for further analysis: surround suppression and adaptation. We show that both mechanisms work to filter the neural signals provided by the superior colliculus, a mid-brain area important for directing behaviour. We also show that the two mechanisms are unexpectedly intertwined, endowing rich dynamics on neural signals at the first central stage of sensory processing. Finally, our results suggest a subpopulation of neurons that is specialised for signalling the presence of potentially important objects.
Footnotes
Authors report no conflict of interest.
S.G.S. received support from a project grant from the Biotechnology and Biological Sciences Research Council (BB/R004765/1), and an International Collaboration Award (with Adam Kohn) from the Stavros Niarchos Foundation / Research to Prevent Blindness. G.D.F. was also supported by an Impact studentship from UCL.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
Jump to comment: