Dynamic Distortion of Orientation Representation after Learning in the Mouse Primary Visual Cortex.

Learning is an essential cognitive mechanism allowing behavioral adaptation through adjustments in neuronal processing. It is associated with changes in the activity of sensory cortical neurons evoked by task-relevant stimuli. However, the exact nature of those modifications and the computational advantages they may confer are still debated. Here, we investigated how learning an orientation discrimination task alters the neuronal representations of the cues orientations in the primary visual cortex (V1) of male and female mice. When comparing the activity evoked by the task stimuli in naive mice and the mice performing the task, we found that the representations of the orientation of the rewarded and nonrewarded cues were more accurate and stable in trained mice. This better cue representation in trained mice was associated with a distortion of the orientation representation space such that stimuli flanking the task-relevant orientations were represented as the task stimuli themselves, suggesting that those stimuli were generalized as the task cues. This distortion was context dependent as it was absent in trained mice passively viewing the task cues and enhanced in the behavioral sessions where mice performed best. Those modifications of the V1 population orientation representation in performing mice were supported by a suppression of the activity of neurons tuned for orientations neighboring the orientations of the task cues. Thus, visual processing in V1 is dynamically adapted to enhance the reliability of the representation of the learned cues and favor generalization in the task-relevant computational space.SIGNIFICANCE STATEMENT Performance improvement in a task often requires facilitating the extraction of the information necessary to its execution. Here, we demonstrate the existence of a suppression mechanism that improves the representation of the orientations of the task stimuli in the V1 of mice performing an orientation discrimination task. We also show that this mechanism distorts the V1 orientation representation space, leading stimuli flanking the task stimuli orientations to be generalized as the task stimuli themselves.

Pure tones modulate the representation of orientation and direction in the primary visual cortex.

Multimodal sensory integration facilitates the generation of a unified and coherent perception of the environment. It is now well established that unimodal sensory perceptions, such as vision, are improved in multisensory contexts. Whereas multimodal integration is primarily performed by dedicated multisensory brain regions such as the association cortices or the superior colliculus, recent studies have shown that multisensory interactions also occur in primary sensory cortices. In particular, sounds were shown to modulate the responses of neurons located in layers 2/3 (L2/3) of the mouse primary visual cortex (V1). Yet, the net effect of sound modulation at the V1 population level remained unclear. In the present study, we performed two-photon calcium imaging in awake mice to compare the representation of the orientation and the direction of drifting gratings by V1 L2/3 neurons in unimodal (visual only) or multimodal (audiovisual) conditions. We found that sound modulation depended on the tuning properties (orientation and direction selectivity) and response amplitudes of V1 L2/3 neurons. Sounds potentiated the responses of neurons that were highly tuned to the cue's orientation and direction but weakly active in the unimodal context, following the principle of inverse effectiveness of multimodal integration. Moreover, sound suppressed the responses of neurons untuned for the orientation and/or the direction of the visual cue. Altogether, sound modulation improved the representation of the orientation and direction of the visual stimulus in V1 L2/3. Namely, visual stimuli presented with auditory stimuli recruited a neuronal population better tuned to the visual stimulus orientation and direction than when presented alone. NEW & NOTEWORTHY The primary visual cortex (V1) receives direct inputs from the primary auditory cortex. Yet, the impact of sounds on visual processing in V1 remains controverted. We show that the modulation by pure tones of V1 visual responses depends on the orientation selectivity, direction selectivity, and response amplitudes of V1 neurons. Hence, audiovisual stimuli recruit a population of V1 neurons better tuned to the orientation and direction of the visual stimulus than unimodal visual stimuli.

Estimating How Sounds Modulate Orientation Representation in the Primary Visual Cortex Using Shallow Neural Networks.

Audiovisual perception results from the interaction between visual and auditory processing. Hence, presenting auditory and visual inputs simultaneously usually improves the accuracy of the unimodal percepts, but can also lead to audiovisual illusions. Cross-talks between visual and auditory inputs during sensory processing were recently shown to occur as early as in the primary visual cortex (V1). In a previous study, we demonstrated that sounds improve the representation of the orientation of visual stimuli in the naïve mouse V1 by promoting the recruitment of neurons better tuned to the orientation and direction of the visual stimulus. However, we did not test if this type of modulation was still present when the auditory and visual stimuli were both behaviorally relevant. To determine the effect of sounds on active visual processing, we performed calcium imaging in V1 while mice were performing an audiovisual task. We then compared the representations of the task stimuli orientations in the unimodal visual and audiovisual context using shallow neural networks (SNNs). SNNs were chosen because of the biological plausibility of their computational structure and the possibility of identifying post hoc the biological neurons having the strongest influence on the classification decision. We first showed that SNNs can categorize the activity of V1 neurons evoked by drifting gratings of 12 different orientations. Then, we demonstrated using the connection weight approach that SNN training assigns the largest computational weight to the V1 neurons having the best orientation and direction selectivity. Finally, we showed that it is possible to use SNNs to determine how V1 neurons represent the orientations of stimuli that do not belong to the set of orientations used for SNN training. Once the SNN approach was established, we replicated the previous finding that sounds improve orientation representation in the V1 of naïve mice. Then, we showed that, in mice performing an audiovisual detection task, task tones improve the representation of the visual cues associated with the reward while deteriorating the representation of non-rewarded cues. Altogether, our results suggest that the direction of sound modulation in V1 depends on the behavioral relevance of the visual cue.