Summary: Findings reveal the brain may optimize visual information processing depending on its conscious state.
Source: Kyoto University
What we see in front of us is what our brains tell us it sees. Our eyes capture visual stimuli which are converted into an image, to which the brain responds by organizing neurons into clusters. These clusters are found in many brain regions, for example, the visual cortex and the superior colliculus.
A new study by Kyoto University researchers, appearing in the Journal of Neuroscience, shows that clusters in the superior colliculus dynamically change depending on whether a mouse is awake or anesthetized. These findings suggest that the brain may optimize visual information processing depending on its conscious state.
The superior colliculus, which is older in terms of evolution, is typically less studied and considered less vital for visual perception even though it is responsible for saccades, rapid eye movement between two fixed points, as well as facial recognition.
Visual information is represented as a map-like spatial response pattern for efficient information processing. These patterns respond to the direction and orientation of the visual image. However, the properties of these spatial pattern maps are not well understood, as different research groups have come to differing conclusions.
“We revealed that these map- or cluster-like representations of moving directions were enhanced in isoflurane anesthesia,” says Masatoshi Kasai, one of the authors of the study.
Suspecting that different brain states were the reason, Kasai and co-author Tadashi Isa, of KyotoU’s WPI-ASHBi, used two-photon microscope calcium imaging to model the different states in mouse brains while they were awake or sedated.
Compared to the awake state, more neurons responded to specific orientations under anesthesia, demonstrating an unexpected dynamic of the mapping that allows the superior colliculus to adapt.
Kasai notes, “Usually, functional maps in the cortex are stable once they are formed.”
He adds that his results, however, suggest the clustering of neurons in the superior colliculus changes in response to the condition of the brain to process visual information efficiently.”
The anesthetic isoflurane was chosen as it suppresses the GABAergic inhibitor neurons, whereas other types do not. The isoflurane-influenced dynamics in the pattern mapping, unseen with other anesthetics, also suggest that “the superior colliculus is more involved in vision information processing than previously thought,” says Kasai.
The superior colliculus (SC) is the midbrain center for integrating visual and multimodal sensory information. Neurons in the SC exhibit direction and orientation selectivity. Recent studies reported that neurons with similar preferences formed clusters in the mouse SC (Feinberg and Meister, 2014; Ahmadlou and Heimel, 2015; de Malmazet et al., 2018; Li et al., 2020) However, it remains controversial as to how these clusters are organized within the SC (Inayat et al., 2015; Chen et al., 2021).
Here, we found that different brain states (i.e., awake or anesthetized with isoflurane) changed selectivity of individual SC neurons and organizations of the neuronal population in both male and female mice. Using two-photon Ca2+ imaging, we examined both individual neuronal responses and the spatial patterns of their population responses. Under isoflurane anesthesia, orientation selectivity increased and a larger number of orientation-selective cells were observed when compared to the awake condition, whereas the proportions of direction-selective cells were similar in both conditions.
Furthermore, direction- and orientation-selective cells located at closer positions showed more similar preferences, and cluster-like spatial patterns were enhanced. Inhibitory responses of direction selective neurons were also reduced under isoflurane anesthesia. Thus, the changes in the spatial organization of response patterns were considered to be due to changes in the balance of excitation and inhibition, with excitation dominance, in the local circuits.
These results provide new insights into the possibility that the functional organization of feature selectivity in the brain is affected by brain state.
Recent large-scale recording studies are changing our view of visual maps in the superior colliculus (SC), including findings of cluster-like localizations of direction- and orientation-selective neurons. However, results from several laboratories are conflicting regarding the presence of cluster-like organization.
Here, we demonstrated that light isoflurane anesthesia affected the direction- and orientation-tuning properties in the mouse superficial SC and that their cluster-like localization pattern was enhanced by the anesthesia. Furthermore, the effect of anesthesia on direction selectivity appeared to be different in the excitatory and inhibitory populations in the SC.
Our results suggest that the functional organization of direction and orientation selectivity might be regulated by the excitation-inhibition balance that depends on the brain state.