The mouse is a promising model in the study of visual system function and development because of available genetic tools. However, a quantitative analysis of visual receptive field properties had not been performed in the mouse superior colliculus (SC) despite its importance in mouse vision and its usefulness in developmental studies. We have made single-unit extracellular recordings from superficial layers of the SC in urethane-anesthetized C57BL/6 mice. We first map receptive fields with flashing spot stimuli and show that most SC neurons have spatially overlapped ON and OFF subfields. With drifting sinusoidal gratings, we then determine the tuning properties of individual SC neurons, including selectivity for stimulus direction and orientation, spatial frequency tuning, temporal frequency tuning, response linearity, and size preference. A wide range of receptive field sizes and selectivity are observed across the population and in various subtypes of SC neurons identified morphologically. In particular, orientation-selective responses are discovered in the mouse SC, and they are not affected by cortical lesion or long-term visual deprivation. However, ON/OFF characteristics and spatial frequency tuning of SC neurons are influenced by cortical inputs and require visual experience during development. Together, our results provide essential information for future investigations on the functional development of the superior colliculus.

SUMMARY Changes of ocular dominance in the visual cortex can be induced by visual manipulations during a critical period in early life. However, the role of critical period plasticity in normal development is unknown. Here we show that at the onset of this time window, the preferred orientations of individual cortical cells in the mouse are mismatched through the two eyes and the mismatch decreases and reaches adult levels by the end of the period. Deprivation of visual experience during this period irreversibly blocks the binocular matching of orientation preference, but has no effect in adulthood. The critical period of binocular matching can be delayed by long-term visual deprivation from birth, like that of ocular dominance plasticity. These results demonstrate that activity-dependent changes induced by normal visual experience during the well-studied critical period serve to match eye-specific inputs in the cortex, thus revealing a physiological role for critical period plasticity during normal development.

Neurons of the cerebellar nuclei (CbN), which generate cerebellar output, are inhibited by Purkinje cells. With extracellular recordings during voluntary locomotion in head-fixed mice, we tested how the rate and coherence of inhibition influence CbN cell firing and well-practiced movements. Firing rates of Purkinje and CbN cells were modulated systematically through the stride cycle (~200–300 ms). Optogenetically stimulating ChR2-expressing Purkinje cells with light steps or trains evoked either asynchronous or synchronous inhibition of CbN cells. Steps slowed CbN firing. Trains suppressed CbN cell firing less effectively, but consistently altered millisecond-scale spike timing. Steps or trains that perturbed stride-related modulation of CbN cell firing rates correlated well with irregularities of movement, suggesting that ongoing locomotion is sensitive to alterations in modulated CbN cell firing. Unperturbed locomotion continued more often during trains than steps, however, suggesting that stride-related modulation of CbN spiking is less readily disrupted by synchronous than asynchronous inhibition.

Retinotopic mapping is a basic feature of visual system organization, but its role in processing visual information is unknown. Mutant mice lacking the ␤2 subunit of nicotinic acetylcholine receptor have imprecise maps in both visual cortex (V1) and the superior colliculus (SC) due to the disruption of spontaneous retinal activity during development. Here, we use behavioral and physiological approaches to study their visual functions. We find that ␤2Ϫ/Ϫ mice fail to track visual stimuli moving along the nasotemporal axis in a subcortical optomotor behavior, but track normally along the dorsoventral axis. In contrast, these mice display normal acuity along both axes in the visual water task, a behavioral test of cortical functions. Consistent with the behavioral results, we find that V1 neurons in ␤2Ϫ/Ϫ mice have normal response properties, while SC neurons have disrupted receptive fields, including enlarged structure and decreased direction and orientation selectivity along the nasotemporal axis. The subcortical-specific deficits indicate that retinotopic map disruption has different impacts on the development of functional properties in V1 and the SC.

The convergence of eye-specific thalamic inputs to visual cortical neurons forms the basis of binocular vision. Inputs from the same eye that signal light increment (On) and decrement (Off) are spatially segregated into subregions, giving rise to cortical receptive fields (RFs) that are selective for stimulus orientation. Here we map RFs of binocular neurons in the mouse primary visual cortex using spike-triggered average. We find that subregions of the same sign (On-On and Off-Off) preferentially overlap between the 2 monocular RFs, leading to binocularly matched orientation tuning. We further demonstrate that such subregion correspondence and the consequent matching of RF orientation are disrupted in mice reared in darkness during development. Surprisingly, despite the lack of all postnatal visual experience, a substantial degree of subregion correspondence still remains. In addition, dark-reared mice show normal monocular RF structures and binocular overlap. These results thus reveal the specific roles of experience-dependent and -independent processes in binocular convergence and refinement of On and Off inputs onto single cortical neurons.