Visual Receptive Field Properties of Neurons in the Superficial Superior Colliculus of the Mouse

Abstract

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.

GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

“…On the other hand, while CGP injection did not affect the peak firing rate (predrug, 115.4 ± 19.2 Hz vs. CGP, 143.4 ± 25.9 Hz, n = 5; P = 0.124; Fig. 4C1-3 (Dräger and Hubel, 1975;Rhoades and Chalupa, 1977;Wang et al, 2010), cats Cynader, 1972, 1975), and monkeys (Schiller and Koerner, 1971;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Marrocco and Li, 1977;Moors and Vendrik, 1979), although they did not explicitly describe the pause between the ON and OFF responses. With the use of juxtacellular labeling, we revealed that the ON + Pause + OFF responses were observed in a variety of morphological types of sSC neurons.…”

“…The majority of sSC neurons reportedly exhibit both ON and OFF responses in response to a static visual stimulus (Schiller and Koerner, 1971; Cynader, 1972, 1975;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Dräger and Hubel, 1975;Marrocco and Li, 1977;Rhoades and Chalupa, 1977;Moors and Vendrik, 1979;Wang et al, 2010).…”

“…The sSC contains silent neurons that fire only when a visual stimulus is presented (Dräger and Hubel, 1975;Marrocco and Li, 1977;Rhoades and Chalupa, 1977;Wang et al, 2010). One of the methods used to detect inhibitory inputs in these neurons is direct measurement of hyperpolarizing currents or membrane potential changes with whole-cell or intracellular recordings (Tao and Poo, 2005;Lien et al, 2006).…”

“…The superficial layer of the SC (sSC) receives visual inputs from the retina and the primary visual cortex (V1) in a retinotopically organized manner (Dräger and Hubel, 1976;May, 2006). sSC neurons exhibit transient spike discharges, called ON responses, immediately after the appearance of a visual stimulus (Schiller and Koerner, 1971; Cynader, 1972, 1975;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Dräger and Hubel, 1975;Rhoades and Chalupa, 1977;Marrocco and Li, 1977;Moors and Vendrik, 1979;Wang et al, 2010), implying that the sSC could detect the appearance of the object. Indeed, lesions or inactivation of the SC cause a detection deficit of visual stimuli (Butter et al, 1978;Overton and Dean, 1988;Fitzmaurice et al, 2003).…”

“…These findings are of particular importance because both excitatory and inhibitory neurons exhibited the same response pattern, although their functions must be different from each other: as 20 excitatory sSC neurons are projection neurons (Mooney et al, 1988;Isa et al, 1998;Özen et al, 2000;Kaneda et al, 2008), they send visual information to nuclei outside the sSC. On the other hand, given that the majority of GABAergic neurons are interneurons with some exceptions (Mooney et al, 1988), their primary role is most likely to inhibit excitatory and inhibitory neurons within the sSC.The sSC contains silent neurons that fire only when a visual stimulus is presented (Dräger and Hubel, 1975;Marrocco and Li, 1977;Rhoades and Chalupa, 1977;Wang et al, 2010). One of the methods used to detect inhibitory inputs in these neurons is direct measurement of hyperpolarizing currents or membrane potential changes with whole-cell or intracellular recordings (Tao and Poo, 2005;Lien et al, 2006).…”