Amygdala Underlies the Environment Dependency of Defense Responses Induced via Superior Colliculus

In our previous study, we showed that the defense responses induced by the selective optogenetic activation of the uncrossed output pathway from the deeper layer of the superior colliculus were environment dependent in the mouse. In a small closed box, the stimulus frequently induced flight (fast forward run away) responses, while in a large open field, the stimulus tended to induce backward retreat responses. We tested a hypothesis that the amygdala is involved in such environment dependency of the innate defense responses. For this purpose, we made a bilateral lesion of the amygdala induced by the ibotenic acid injections in male mice. As a result, in the mice with lesions of substantial portions of the basolateral and basomedial complex, the flight responses in the closed box disappeared and retreat responses were mainly induced. The retreat responses on the open platform were unchanged. Classically, the amygdala has been considered to be involved in the memory-dependent contextual modulation of the fear responses. In contrast, the present results suggest a novel view on the role of the amygdala in which the amygdala plays a key role in sensing the current environmental setting for making a quick decision of action upon emergency, which is critical for survival in the natural environment.

Superior colliculus drives stimulus-evoked directionally biased saccades and attempted head movements in head-fixed mice

Animals investigate their environments by directing their gaze towards salient stimuli. In the prevailing view, mouse gaze shifts entail head rotations followed by brainstem-mediated eye movements, including saccades to reset the eyes. These 'recentering' saccades are attributed to head movement-related vestibular cues. However, microstimulating mouse superior colliculus (SC) elicits directed head and eye movements resembling SC-dependent sensory-guided gaze shifts in other species, suggesting that mouse gaze shifts may be more flexible than has been recognized. We investigated this possibility by tracking eye and attempted head movements in a head-fixed preparation that eliminates head movement-related sensory cues. We found tactile stimuli evoke directionally biased saccades coincident with attempted head rotations. Differences in saccade endpoints across stimuli are associated with distinct stimulus-dependent relationships between initial eye position and saccade direction and amplitude. Optogenetic perturbations revealed SC drives these gaze shifts. Thus, head-fixed mice make sensory-guided, SC-dependent gaze shifts involving coincident, directionally biased saccades and attempted head movements. Our findings uncover flexibility in mouse gaze shifts and provide a foundation for studying head-eye coupling.

Nonlinear visuoauditory integration in the mouse superior colliculus

Sensory information from different modalities is processed in parallel, and then integrated in associative brain areas to improve object identification and the interpretation of sensory experiences. The Superior Colliculus (SC) is a midbrain structure that plays a critical role in integrating visual, auditory, and somatosensory input to assess saliency and promote action. Although the response properties of the individual SC neurons to visuoauditory stimuli have been characterized, little is known about the spatial and temporal dynamics of the integration at the population level. Here we recorded the response properties of SC neurons to spatially restricted visual and auditory stimuli using large-scale electrophysiology. We then created a general, population-level model that explains the spatial, temporal, and intensity requirements of stimuli needed for sensory integration. We found that the mouse SC contains topographically organized visual and auditory neurons that exhibit nonlinear multisensory integration. We show that nonlinear integration depends on properties of auditory but not visual stimuli. We also find that a heuristically derived nonlinear modulation function reveals conditions required for sensory integration that are consistent with previously proposed models of sensory integration such as spatial matching and the principle of inverse effectiveness.

Functional Organisation of the Mouse Superior Colliculus

The superior colliculus (SC) is a highly conserved area of the mammalian midbrain that is widely implicated in the organisation and control of behaviour. SC receives input from a large number of brain areas, and provides outputs to a large number of areas. The convergence and divergence of anatomical connections with different areas and systems provides challenges for understanding how SC contributes to behaviours. Recent work in mouse has provided large anatomical datasets, and a wealth of new data from experiments that identify and manipulate different cells within SC, and its inputs and outputs. These data offer an opportunity to better understand the functional roles of SC. However, some of the observations appear, at first sight, to be contradictory. Here we review this recent work and suggest a simple framework which can capture the observations, and that requires only a small change to previous models. Specifically, the functional organisation of SC can be explained by supposing that three largely distinct circuits support three largely distinct classes of behaviour - arrest, turning towards, and the triggering of escape or pursuit. These behavioural classes are supported by the optic, intermediate and deep layers respectively.