The superior colliculus is a conserved sensorimotor structure that integrates visual and other sensory information to drive reflexive behaviors. Although the evidence for this is strong and compelling, a number of experiments reveal a role for the superior colliculus in behaviors usually associated with the cerebral cortex, such as attention and decision-making. Indeed, in addition to collicular outputs targeting brainstem regions controlling movements, the superior colliculus also has ascending projections linking it to forebrain structures including the basal ganglia and amygdala, highlighting the fact that the superior colliculus, with its vast inputs and outputs, can influence processing throughout the neuraxis. Today, modern molecular and genetic methods combined with sophisticated behavioral assessments have the potential to make significant breakthroughs in our understanding of the evolution and conservation of neuronal cell types and circuits in the superior colliculus that give rise to simple and complex behaviors.

Motion streaks are smeared representation of fast-moving objects due to temporal integration. Here, we test for motion streak signals in mice with two-photon calcium imaging. For small dots moving at low speeds, neurons in primary visual cortex (V1) encode the component motion, with preferred direction along the axis perpendicular to their preferred orientation. At high speeds, V1 neurons prefer the direction along the axis parallel to their preferred orientation, as expected for encoding motion streaks. Whereas some V1 neurons (∼20%) display a switch of preferred motion axis with increasing speed, others (>40%) respond specifically to high speeds at the parallel axis. Motion streak neurons are also seen in higher visual lateromedial (LM), anterolateral (AL), and rostrolateral (RL) areas, but with higher transition speeds, and many still prefer the perpendicular axis even with fast motion. Our results thus indicate that diverse motion encoding exists in mouse visual cortex, with intriguing differences among visual areas.

Neurons in the visual system can be spatially organized according to their response properties such as receptive field location and feature selectivity. For example, the visual cortex of many mammalian species contains orientation and direction columns where neurons with similar preferences are clustered. Here, we examine whether such a columnar structure exists in the mouse superior colliculus (SC), a prominent visual center for motion processing. By performing large-scale physiological recording and two-photon calcium imaging in adult male and female mice, we show that direction-selective neurons in the mouse SC are not organized into stereotypical columns as a function of their preferred directions, although clusters of similarly tuned neurons are seen in a minority of mice. Nearby neurons can prefer similar or opposite directions in a largely position-independent manner. This finding holds true regardless of animal state (anesthetized vs awake, running vs stationary), SC depth (most superficial lamina vs deeper in the SC), research technique (calcium imaging vs electrophysiology), and stimulus type (drifting gratings vs moving dots, full field vs small patch). Together, these results challenge recent reports of region-specific organizations in the mouse SC and reveal how motion direction is represented in this important visual center.

In mouse visual cortex, right after eye opening binocular cells have different preferred orientations for input from the two eyes. With normal visual experience during a critical period, these preferred orientations evolve and eventually become well matched. To gain insight into the matching process, we developed a computational model of a cortical cell receiving orientation selective inputs via plastic synapses. The model captures the experimentally observed matching of the preferred orientations, the dependence of matching on ocular dominance of the cell, and the relationship between the degree of matching and the resulting monocular orientation selectivity. Moreover, our model puts forward testable predictions: 1) The matching speed increases with initial ocular dominance. 2) While the matching improves more slowly for cells that are more orientation selective, the selectivity increases faster for better matched cells during the matching process. This suggests that matching drives orientation selectivity but not vice versa. 3) There are two main routes to matching: the preferred orientations either drift toward each other or one of the orientations switches suddenly. The latter occurs for cells with large initial mismatch and can render the cells monocular. We expect that these results provide insight more generally into the development of neuronal systems that integrate inputs from multiple sources, including different sensory modalities.NEW & NOTEWORTHY Animals gather information through multiple modalities (vision, audition, touch, etc.). These information streams have to be merged coherently to provide a meaningful representation of the world. Thus, for neurons in visual cortex V1, the orientation selectivities for inputs from the two eyes have to match to enable binocular vision. We analyze the postnatal process underlying this matching using computational modeling. It captures recent experimental results and reveals interdependence between matching, ocular dominance, and orientation selectivity.

Visual responses are extensively shaped by internal factors. This effect is drastic in the primary visual cortex (V1), where locomotion profoundly increases visually-evoked responses. Here we investigate whether a similar effect exists in another major visual structure, the superior colliculus (SC). By performing 2-photon calcium imaging of head-fixed male and female mice running on a treadmill, we find that only a minority of neurons in the most superficial lamina of the SC display significant changes during locomotion. This modulation includes both increase and decrease in response amplitude and is similar between excitatory and inhibitory neurons. The overall change in the SC is small, whereas V1 responses almost double during locomotion. Additionally, SC neurons display lower response variability and less spontaneous activity than V1 neurons. Together, these experiments indicate that locomotion-dependent modulation is not a widespread phenomenon in the early visual system and that SC and V1 use different strategies to encode visual information.SIGNIFICANCE STATEMENTVisual information captured by the retina is processed in parallel through two major pathways, one reaching the primary visual cortex through the thalamus, and the other projecting to the superior colliculus. The two pathways then merge in the higher areas of the visual cortex. Recent studies have shown that behavioral state such as locomotion is an essential component of vision and can strongly affect visual responses in the thalamocortical pathway. Here we demonstrate that neurons in the mouse superior colliculus and primary visual cortex display striking differences in their modulation by locomotion, as well as in response variability and spontaneous activity. Our results reveal an important "division of labor" in visual processing between these two evolutionarily distinct structures.

The superior colliculus (SC) is the most prominent visual center in mice. Studies over the past decade have greatly advanced our understanding of the function, organization, and development of the mouse SC, which has rapidly become a popular model in vision research. These studies have described the diverse and cell-type-specific visual response properties in the mouse SC, revealed their laminar and topographic organizations, and linked the mouse SC and downstream pathways with visually guided behaviors. Here, we summarize these findings, compare them with the rich literature of SC studies in other species, and highlight important gaps and exciting future directions. Given its clear importance in mouse vision and the available modern neuroscience tools, the mouse SC holds great promise for understanding the cellular, circuit, and developmental mechanisms that underlie visual processing, sensorimotor transformation, and, ultimately, behavior.

Neural circuits are shaped by experience during critical periods of development. Sensory deprivation during these periods permanently compromises an organism's ability to perceive the outside world. In the mouse visual system, normal visual experience during a critical period in early life drives the matching of individual cortical neurons' orientation preferences through the two eyes, likely a key step in the development of binocular vision. Here, in mice of both sexes, we show that the binocular matching process is completely blocked by monocular deprivation spanning the entire critical period. We then show that 3 weeks of environmental enrichment (EE), a paradigm of enhanced sensory, motor, and cognitive stimulation, is sufficient to rescue binocular matching to the level seen in unmanipulated mice. In contrast, 6 weeks of conventional housing only resulted in a partial rescue. Finally, we use two-photon calcium imaging to track the matching process chronically in individual cells during EE-induced rescue. We find that for cells that are clearly dominated by one of the two eyes, the input representing the weaker eye changes its orientation preference to align with that of the dominant eye. These results thus reveal ocular dominance as a key driver of the binocular matching process, and suggest a model whereby the dominant input instructs the development of the weaker input. Such a mechanism may operate in the development of other systems that need to integrate inputs from multiple sources to generate normal neuronal functions.SIGNIFICANCE STATEMENT Critical periods are developmental windows of opportunity that ensure the proper wiring of neural circuits, as well as windows of vulnerability when abnormal experience could cause lasting damage to the developing brain. In the visual system, critical period plasticity drives the establishment of binocularly matched orientation preferences in cortical neurons. Here, we show that binocular matching is completely blocked by monocular deprivation during the critical period. Moreover, environmental enrichment can fully rescue the disrupted matching, whereas conventional housing of twice the duration results in a partial rescue. We then use two-photon calcium imaging to track individual cells chronically during the EE-induced recovery, and reveal important insights into how appropriate function can be restored to the nervous system after the critical period.