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Allen, K. M.

Publications and source records attributed to Allen, K. M..

5 recordsLinked to original sources

A binocular perception deficit characterizes prey pursuit in developing mice

The mouse continues to be one of the most powerful models in which to address the molecular and cellular mechanisms underlying mammalian visual system development. In particular, integration of binocular information at the cellular level has long been studied in specific regions of the mouse visual cortex to gain mechanistic insight into the development of vision. However, we lack an understanding of the development of the visual perceptions themselves in mice and other species that might rely on successful binocular integration. Further, the superior colliculus also processes binocular input and it remains unclear how early visual experience differentially impacts activity in this brain area during behavior. To address these major outstanding questions, we quantified the natural visually-guided behavior of postnatal day 21 (P21) and adult mice using a live prey capture assay and a computerized-spontaneous perception of visual objects tasks (C-SPOT). Analysis of both behavioral assays revealed robust and specific binocular visual field processing deficits in P21 mice as compared to adults. In addition, c-Fos expression in the anterior region of the superior colliculus (SC), the region that would process stimuli located in the binocular visual field, was highly different between P21 mice and adults after C-SPOT. We thus exploited a natural visual pursuit behavior and C-SPOT to provide the first demonstration of a specific visual perception deficit related to binocular integration in developing mice. HighlightsO_LIJuvenile (P21) mice robustly investigate live insects C_LIO_LIInsect pursuit behavior relying on binocular vision is immature in P21 mice C_LIO_LIVisually-induced arrest responses are similar between P21 and adult mice. C_LIO_LIEthologically-relevant visual experience differentially increases c-Fos expression in the superior colliculus of juveniles versus adults. C_LI

animal behavior and cognition↗

Experience-dependent refinement of natural appetitive visual behavior in mice

Specific features of visual objects innately draw orienting and approach responses in animals, and provide natural signals of potential reward. In addition, the rapid refinement of innate approach responses enhances the ability of an animal to effectively and conditionally forage, capture prey or initiate a rewarding social experience. However, the neural mechanisms underlying how the brain encodes naturally appetitive stimuli and conditionally transforms stimuli into approach behavior remain unclear. As a first step towards this goal, we have developed a behavioral assay to quantify innate, visually-evoked approach behaviors in freely moving mice presented with simple, computer generated stimuli of varying sizes and speeds in the lower visual field. We found that specific combinations of stimulus features selectively evoked innate approach versus freezing behavioral responses. Surprisingly, we also discovered that prey capture experience selectively modified a range of visually-guided appetitive behaviors, including increasing the probability of approach and pursuit of moving stimuli, as well as altering those visual features that evoked approach. These findings will enable the use of sophisticated genetic strategies to uncover novel neural mechanisms underlying predictive coding, innate behavioral choice, and flexible, state-dependent processing of stimuli in the mouse visual system. HighlightsO_LINovel stimuli with specific visual features reliably elicit an approach in C57BL/6J mice. C_LIO_LIIntroduction of motion to stimuli makes freezing the most probable behavioral response. C_LIO_LISpontaneous behavioral responses are tuned to size, speed and visual field location. C_LIO_LIPrey capture experience selectively refines natural, visually-evoked approach behaviors. C_LI

animal behavior and cognition↗

Differences in sodium channel densities in the apical dendrites of pyramidal cells of the electrosensory lateral line lobe.

Heterogeneity of neural properties within a given neural class is ubiquitous in the nervous system and permits different sub-classes of neurons to specialize for specific purposes. This principle has been thoroughly investigated in the hindbrain of the weakly electric fish A. leptorhynchus in the primary electrosensory area, the Electrosensory Lateral Line lobe (ELL). The pyramidal cells that receive inputs from tuberous electroreceptors are organized in three maps in distinct segments of the ELL. The properties of these cells vary greatly across maps due to differences in connectivity, receptor expression, and ion channel composition. These cells are a seminal example of bursting neurons and their bursting dynamic relies on the presence of voltage-gated Na+ channels in the extensive apical dendrites of the superficial pyramidal cells. Other ion channels can affect burst generation and their expression varies across ELL neurons and segments. For example, SK channels cause hyperpolarizing after-potentials decreasing the likelihood of bursting, yet bursting propensity is similar across segments. We question whether the depolarizing mechanism that generates the bursts presents quantitative differences across segments that could counterbalance other differences having the opposite effect. Although their presence and role are established, the distribution and density of the apical dendrites Na+ channels have not been quantified and compared across ELL maps. Therefore, we test the hypothesis that Na+ channel density varies across segment by quantifying their distribution in the apical dendrites of immunolabeled ELL sections. We found the Na+ channels to be two-fold denser in the lateral segment than in the centro-medial segment, the centro-lateral segment being intermediate. Our results imply that this differential expression of voltage-gated Na+ channels could counterbalance or interact with other aspects of neuronal physiology that vary across segments (e.g. SK channels). We argue that burst coding of sensory signals, and the way the network regulates bursting, should be influenced by these variations in Na+ channel density.

neuroscience↗

Simplified neural encoding of social communication reflects lifestyle

As communication signal properties change, through genetic drift or selective pressure, the sensory systems that receive these signals must also adapt to maintain sensitivity and adaptability in an array of contexts. Shedding light on this process helps us understand how sensory codes are tailored to specific tasks. In a species of weakly electric fish, Apteronotus albifrons, we examined the unique neurophysiological properties that support the encoding of electrosensory communication signals that the animal encounters in social exchanges. We compare our findings to known coding properties of the closely related species, Apteronotus leptorhynchus, to establish how these animals differ in their ability to encode their distinctive communication signals. While there are many similarities between these two species, we found notable differences leading to relatively poor coding of the details of chirp structure occurring on high-frequency background beats. As a result, small differences in chirp properties are poorly resolved by the nervous system. We performed behavioral tests to relate A. albifrons chirp coding strategies to its use of chirps during social encounters. Our results suggest that A. albifrons do not exchange frequent chirps in non-breeding condition, particularly when the beat frequency is high. These findings parallel the mediocre chirp coding accuracy in that they both point to a reduced reliance on frequent and rich exchange of information through chirps during these social interactions. Therefore, our study suggests that neural coding strategies in the central nervous system vary across species in a way that parallels the behavioral use of the sensory signals. SIGNIFICANCESender-receiver matching is a phenomenon commonly observed in the peripheral nervous system. It enables communication production and reception to evolve together so that conspecifics remain sensitive to important signals. In this manuscript we examine this phenomenon in the central nervous system of the weakly electric fish A. albifrons and compare its processing of communication signals to a closely related species (A. leptorhynchus). Although some differences across the two species can help tailor the system for processing species-specific signals, our data indicate that encoding of communication signals in A. albifrons is not as sensitive as in A. leptorhynchus for certain categories of signals. Our data support the idea that the extent of sender-receiver matching can vary as a function of behavioral needs.

neuroscience↗

Task-specific sensory coding strategies matched to detection and discrimination behaviors in Apteronotus leptorhynchus

All sensory systems must reliably translate information about the environment into a neural code, mediating perception. The most relevant aspects of stimuli may change as behavioral context changes, making efficient encoding of information more challenging. Sensory systems must balance rapid detection of a stimulus with perception of fine details that enable discrimination between similar stimuli. We show that in a species of weakly electric fish, Apteronotus leptorhynchus, two coding strategies are employed for these separate behavioral tasks. Using communication signals produced in different contexts, we demonstrate a strong correlation between neural coding strategies and behavioral performance on a discrimination task. Extracellular recordings of pyramidal cells within the electrosensory lateral line lobe of alert fish show two distinct response patterns, either burst discharges with little variation between different signals of the same category, or a graded, heterogeneous response that contains enough information to discriminate between signals with slight variations. When faced with a discrimination-based task, the behavioral performance of the fish closely matches predictions based on coding strategy. Comparisons of these results with neural and behavioral responses observed in other model systems suggest that our study highlights a general principle in the way different neural codes are utilized in the sensory system.\n\nSIGNIFICANCE STATEMENTResearch relating the structure of stimuli to the response of sensory neurons has left us with a detailed understanding of how different neural codes can represent information. Although various aspects of neural responses have been related to perceptual abilities, general principles relating behavioral tasks to sensory coding strategies are lacking. A major distinction can be made between signals that must simply be detected versus stimuli that must also be finely discriminated and evaluated. We show that these two different perceptual tasks are systematically matched by distinct neural coding strategies and we argue that our study identifies a general principle that is observed in various sensory systems.\n\nConflict of interest statementThe authors declare no competing financial interests.

neuroscience↗