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Circuits of Visual Attention

Periodic Reporting for period 4 - Daphne (Circuits of Visual Attention)

Reporting period: 2022-06-01 to 2022-11-30

Due to the limited neuronal resources of any nervous system, extracting relevant sensory information from cluttered natural environments is critical to allocate computational power correctly. In this proposal, we explore the neuronal mechanisms used by the nervous system to attend visual cues and thus, enable appropriate behaviors. To do so, we study the visual transformations of the mouse Superior Colliculus (SC), an evolutionarily conserved midbrain area known to process sensorimotor transformations and to be involved in the allocation of attention. By understanding the principles underlying sensorimotor transformation, our work will contribute to building a framework to study attention in health and disease.
The overall objectives of our project are (i) to provide a detailed description of visual representation in the SC, focusing on understanding how defined retinal information-streams, like motion and color, contribute to these properties; (ii) to understand the relationship between motor instructions and sensory coding.
Our published findings show that the visual properties relayed to the SC vary according to efficient coding principles derived from natural statistics and receiving a non-uniform representation of the environment adapted to the animal’s natural environment. Furthermore, in a different study we show, that the timing of perceptual decision-making is regulated via intrinsic excitability of the visuomotor pathway, opening avenues to use innate behaviour to mechanistically dissect cognitive disorders.
Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far (For the final period please include an overview of the results and their exploitation and dissemination)
I. Collective neuronal dynamics of the SC

We developed a paradigm that allows us to image collicular activity in awake behaving animals immersed in a virtual reality arena. While using this system, we unexpectedly observed that neural population activity switches between periods dominated by spatially localized “ordered” hotspots and globally distributed “disordered” patterns (Fig. 1). These switches occur in the presence and absence of visual stimuli. Given that perception results from a dynamic interplay between feed-forward processing of sensory stimuli and spontaneous neural activity, these spontaneous dynamics can be presumed to reflect prior expectations, task demands, and attentional focus. Our analysis has revealed the relationships of these activity patterns that will open doors to study how sensory information is modulated moment-by-moment by the animal state (Mlynarski et al., in preparation).

II. Feed-forward inhibition controls collicular activity based on self-motion cues
The saliency of visual stimuli depends on context, e.g. if the animal is moving or not. Thus, vision can only function properly, if the changes of the visual environment take the interplay between externally and changes due to self-motion into account. We have found, contrary to what was suggested previously, that thalamic projections from the vLGN/IGL complex are tuned to behaviors and visual flows that allow the animal to subtract these at the first visual processing nose in the SC. Using a combination of in vivo awake-behaving paradigms, behavioral analysis and ex-vivo electrophysiology that (i) these thalamic projection is highly specific to the superficial retinorecipient layers (Fig. 2A-B), (ii) are strongly inhibitory influence collicular dynamics, (iii) that information relayed from this thalamic nucleus carries specific information about the animals’ locomotion speed and forward translational optic flow and changes in pupil size and finally, (iv) that these ontogenetically driving these projections can instruct similar behavioral patterns, suggesting a efference-copy like function. Thus, vLGN inhibitions seems to act as a context-specific gain control of visual signals, allowing the animals to suppress predicted increases of visual dynamics due to self-motion (Vega-Zuniga, et al., in preparation).

III. Panoramic view of retinal processing
We developed a theoretical predictive coding framework that indicates that the eye’s computations adapted to the natural statistics of the visual environment. To test this hypothesis, we developed a novel system to image large regions of retinal explants to explore the functional inhomogeneities in retinal receptive field structures, as well as mapping these properties in vivo, in the SC. Our results match our theoretical predictive coding framework, indicating that the eye’s computations adapted to the natural statistics of the visual environment (Fig. 3) (Gupta et al., 2022).

IV. Visuomotor deficits in models of ASD.
Individuals with autism spectrum disorder (ASD) exhibit cognitive difficulties together with impairments in sensory processing. These conditions are believed to arise during cortical neurodevelopment; however, a comprehensive description of neuronal mechanisms liking sensation with behavior remains unclear. Here we show that a subcortical mechanism of sensory processing required to initiate efficient threat responses are disrupted in models of ASD (Fig. 4). This convergent phenotype allowed us to systematically dissect the neuronal dysfunction to a specific node, the dorsal periaqueductal gray. We show that the phenotype emerges due to Kv1.1 mediated hypo-excitability, providing a mechanistic model of cognitive dysfunction from gene to behavior (Burnett et al. 2022).
We have established several independent but complementary approaches to understand sensory processing in the SC. Within these projects, we have shown to be capable of recording large-scale population dynamics in retinas and in the SC, and thoroughly analyze animal behavior, allowing us to differentially assess the contributions of (i) genetically-defined cell types, their projections, (ii) population dynamics, and (iii) their role in instructing behavior. We have explored the homogeneity of visual responses across the retina and SC, and their relationships with natural statistics (Gupta et al., 2022). We have deciphered a specific interplay between behavior and vision at the first visual node in the brain (Vega-Zuniga et al., in preparation). We are found and described a new and prominent type of salient, population-level phenomenon in the SC. In close with a theory group at ISTA (G. Tkacik), we develop new tools and approaches to properly describe it, showing that the superficial SC, beyond being a relay of visual information, combines task demands and attentional focus (Mlynarski et al., in preparation). Finally, we have linked visuomotor deficits as a convergent phonotype in autism models. We described this robust behavioral phenotype and used it to dissected the pathway, showing that subcortical circuit have an important role in ASD.