Natural visual behavior and active sensing in the mouse.

In the natural world, animals use vision for a wide variety of behaviors not reflected in most laboratory paradigms. Although mice have low-acuity vision, they use their vision for many natural behaviors, including predator avoidance, prey capture, and navigation. They also perform active sensing, moving their head and eyes to achieve behavioral goals and acquire visual information. These aspects of natural vision result in visual inputs and corresponding behavioral outputs that are outside the range of conventional vision studies but are essential aspects of visual function. Here, we review recent studies in mice that have tapped into natural behavior and active sensing to reveal the computational logic of neural circuits for vision.

Maternal diet during early gestation influences postnatal taste activity-dependent pruning by microglia.

A key process in central sensory circuit development involves activity-dependent pruning of exuberant terminals. Here, we studied gustatory terminal field maturation in the postnatal mouse nucleus of the solitary tract (NST) during normal development and in mice where their mothers were fed a low NaCl diet for a limited period soon after conception. Pruning of terminal fields of gustatory nerves in controls involved the complement system and is likely driven by NaCl-elicited taste activity. In contrast, offspring of mothers with an early dietary manipulation failed to prune gustatory terminal fields even though peripheral taste activity developed normally. The ability to prune in these mice was rescued by activating myeloid cells postnatally, and conversely, pruning was arrested in controls with the loss of myeloid cell function. The altered pruning and myeloid cell function appear to be programmed before the peripheral gustatory system is assembled and corresponds to the embryonic period when microglia progenitors derived from the yolk sac migrate to and colonize the brain.

Coarse-to-fine processing drives the efficient coding of natural scenes in mouse visual cortex.

The visual system processes sensory inputs sequentially, perceiving coarse information before fine details. Here we study the neural basis of coarse-to-fine processing and its computational benefits in natural vision. We find that primary visual cortical neurons in awake mice respond to natural scenes in a coarse-to-fine manner, primarily driven by individual neurons rapidly shifting their spatial frequency preference from low to high over a brief response period. This shift transforms the population response in a way that counteracts the statistical regularities of natural scenes, thereby reducing redundancy and generating a more efficient neural representation. The increase in representational efficiency does not occur in either dark-reared or anesthetized mice, which show significantly attenuated coarse-to-fine spatial processing. Collectively, these results illustrate that coarse-to-fine processing is state dependent, develops postnatally via visual experience, and provides a computational advantage by generating more efficient representations of the complex spatial statistics of ethologically relevant natural scenes.

Selective Removal of Sodium Salt Taste Disrupts the Maintenance of Dendritic Architecture of Gustatory Relay Neurons in the Mouse Nucleus of the Solitary Tract.

Neuronal activity plays critical roles in the development of sensory circuits in the mammalian brain. Experimental procedures are now available to alter the function of specific taste transduction pathways and have been especially useful in studying how stimulus-specific taste activity influences the development of central gustatory circuits. We previously used a mouse knock-out (KO) model in which the transduction channel necessary for sodium taste is removed from taste bud cells throughout life. In these KO mice, the terminal fields that carry taste information from taste buds into the nucleus of the solitary tract (NST) fail to mature, suggesting that sodium-elicited taste activity is important for the proper development of central gustatory circuits. Here, we tested the hypothesis that the development and maintenance of the dendritic architecture of NST relay cells, the primary postsynaptic partner of gustatory nerve terminal fields, are similarly dependent on sodium-elicited taste activity. The dendritic fields of NST relay cells, from adult male and female mice in which the α-subunit of the epithelial sodium channel (αENaC) was conditionally deleted in taste bud cells throughout life, were up to 2.4× larger and more complex than that of age-matched control mice. Interestingly, these differences in dendritic architecture did not appear until after the age when terminal fields begin "pruning," after postnatal day (P)20. Overall, our results suggest that ENaC-mediated sodium taste activity is necessary for the maintenance of dendritic fields of relay cells in the gustatory NST.

Two Is Greater Than One: Binocular Visual Experience Drives Cortical Orientation Map Alignment.

One hallmark of the mature visual cortex is binocularly matched orientation maps. In this issue of Neuron, Chang et al. (2020) show that three different maps exist at vision onset and that binocular visual experience aligns them into a single unified representation.

Maintenance of Mouse Gustatory Terminal Field Organization Is Disrupted following Selective Removal of Peripheral Sodium Salt Taste Activity at Adulthood.

Neural activity plays a critical role in the development of central circuits in sensory systems. However, the maintenance of these circuits at adulthood is usually not dependent on sensory-elicited neural activity. Recent work in the mouse gustatory system showed that selectively deleting the primary transduction channel for sodium taste, the epithelial sodium channel (ENaC), throughout development dramatically impacted the organization of the central terminal fields of three nerves that carry taste information to the nucleus of the solitary tract. More specifically, deleting ENaCs during development prevented the normal maturation of the fields. The present study was designed to extend these findings by testing the hypothesis that the loss of sodium taste activity impacts the maintenance of the normal adult terminal field organization in male and female mice. To do this, we used an inducible Cre-dependent genetic recombination strategy to delete ENaC function after terminal field maturation occurred. We found that removal of sodium taste neural activity at adulthood resulted in significant reorganization of mature gustatory afferent terminal fields in the nucleus of the solitary tract. Specifically, the chorda tympani and greater superficial petrosal nerve terminal fields were 1.4× and 1.6× larger than age-matched controls, respectively. By contrast, the glossopharyngeal nerve, which is not highly sensitive to sodium taste stimulation, did not undergo terminal field reorganization. These surprising results suggest that gustatory nerve terminal fields remain plastic well into adulthood, which likely impacts central coding of taste information and taste-related behaviors with altered taste experience.SIGNIFICANCE STATEMENT Neural activity plays a major role in the development of sensory circuits in the mammalian brain. However, the importance of sensory-driven activity in maintaining these circuits at adulthood, especially in subcortical structures, appears to be much less. Here, we tested whether the loss of sodium taste activity in adult mice impacts the maintenance of how taste nerves project to the first central relay. We found that specific loss of sodium-elicited taste activity at adulthood produced dramatic and selective reorganization of terminal fields in the brainstem. This demonstrates, for the first time, that taste-elicited activity is necessary for the normal maintenance of central gustatory circuits at adulthood and highlights a level of plasticity not seen in other sensory system subcortical circuits.