Mice Can Use Second-Order, Contrast-Modulated Stimuli to Guide Visual Perception

Abstract

Visual processing along the primate ventral stream takes place in a hierarchy of areas, characterized by an increase in both complexity of neuronal preferences and invariance to changes of low-level stimulus attributes. A basic type of invariance is form-cue invariance, where neurons have similar preferences in response to first-order stimuli, defined by changes in luminance, and global features of second-order stimuli, defined by changes in texture or contrast. Whether in mice, a now popular model system for early visual processing, visual perception can be guided by second-order stimuli is currently unknown. Here, we probed mouse visual perception and neural responses in areas V1 and LM using various types of second-order, contrast-modulated gratings with static noise carriers. These gratings differ in their spatial frequency composition and thus in their ability to invoke first-order mechanisms exploiting local luminance features. We show that mice can transfer learning of a coarse orientation discrimination task involving first-order, luminance-modulated gratings to the contrast-modulated gratings, albeit with markedly reduced discrimination performance. Consistent with these behavioral results, we demonstrate that neurons in area V1 and LM are less responsive and less selective to contrast-modulated than to luminance-modulated gratings, but respond with broadly similar preferred orientations. We conclude that mice can, at least in a rudimentary form, use second-order stimuli to guide visual perception.

Figure-ground perception in the awake mouse and neuronal activity elicited by figure-ground stimuli in primary visual cortex

“…Our results extend a recent study demonstrating that mice can detect the orientation of a grating if it is defined by variations in texture 33 by showing that they can also localize objects defined by an orientation difference. They also complement studies in rats, which are able to recognize objects even if they have undergone transformations such as rotations, size changes or caused by different lighting conditions 16 .…”

Motion Discrimination and the Motion Aftereffect in Mouse Vision

“…Here we examined whether sensory adaptation alters the perception of motion in the mouse. We initiated our experiments by first training animals to discriminate leftward and upward motion using classical conditioning (Khastkhodaei et al, 2016; Jurjut et al, 2017) and then slowly rotated the upward motion to the right until the task was a leftward and rightward motion discrimination. Once mice reached a criterion performance ( d ′ ≥ 0.8) in this task, we measured how the history of sensory stimulation impacted their ability to discriminate these directions.…”

“…The dot lifetime restricted the highest possible coherence to 86% (Bischof et al, 1999). Each trial consisted of a 3 s visual stimulation period and were separated by an interstimulus period lasting 10 s plus a random interval drawn from an exponential distribution with a mean of 10 s. This random interval prevents the mice from predicting the time point of reward delivery (Khastkhodaei et al, 2016; Jurjut et al, 2017). During preliminary motion discrimination training, we displayed dots with 86% coherent motion and 100% Michelson contrast during the stimulation period, and we presented a mean gray screen during the interstimulus period.…”

“…Animals walked on a floating Styrofoam ball while they were head-fixed (Dombeck et al, 2007). Classical conditioning was used to pair visual motion to water delivery (Khastkhodaei et al, 2016; Jurjut et al, 2017). Initially, we presented two different motion conditions, upward and leftward, pairing leftward with a water reward.…”

“…Once trained to associate water with leftward motion, the mice quickly adapted (typically less than a few days) to small changes in the experimental paradigm (e.g., changes in the direction of unrewarded stimuli, coherence, adapting experiments). Licking was measured using a piezoelectric sensor attached to the reward delivery system (Schwarz et al, 2010; Khastkhodaei et al, 2016; Jurjut et al, 2017). The water was delivered in a flexible catheter that would bend upward and downward as the mouse licked.…”