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Hoy, J. L.

Publications and source records attributed to Hoy, J. L..

5 recordsLinked to original sources

GO, NO-GO: A SENSITIVE PERIOD FOR DEVELOPING SEX-SPECIFIC VISUALLY-GUIDED PREY PURSUIT-PREDATOR AVOIDANCE TRADE-OFF STRATEGIES

In natural environments, animals face a trade-off between foraging and staying vigilant against predators, a conflict known to shape sensory processing and behavior through natural selection. Even within a species, this trade-off may be resolved differently depending on age, sex, or life history. To identify the neural mechanisms underlying visually-guided pursuit-avoidance trade-offs, we studied how mice responded to a sudden overhead threat while pursuing a moving, prey-like target near the ground. This paradigm let us quantify orienting decisions in adolescent and adult mice of both sexes. We found that adolescence is a key period when male and female mice begin to diverge in how they resolve this conflict. Manipulating the value of the pursued target during adolescence versus adulthood revealed that adolescence is also a sensitive period for shaping adult escape-to-shelter versus continue to approach target behavior. Notably, hunting experience gained specifically during adolescence caused males, but not females, to shift strategy: experienced adolescent males tended to uniquely shift towards a "no-go" (stay-near-Prey) strategy. All the other groups instead favored an active "go" strategy, repeatedly shifting between approaching target and running to shelter. All mice showed this oscillation between approaching target and escaping to a shelter to some degree, but hunting experience during adolescence most significantly shifted this balance between approach and escape for males.

neuroscience↗

SEXUAL-DIMORPHISM IN VISUALLY GUIDED APPROACH BEHAVIOR EMERGES UNIQUELY DURING ADOLESCENCE

Studying prey capture behavior in mice offers a fruitful platform for understanding how ecologically relevant visual stimuli are differentially processed by the brain throughout life. For example, specific visual stimuli that indicate prey and that naturally draw appetitive orienting in the adult may be interpreted differently or evoke distinct behaviors during development. What are the neural mechanisms that might allow an animal to flexibly couple the same stimulus information to distinct behavioral outcomes as a function of developmental needs? To begin to address this important question, we quantified visually evoked orienting behaviors between adolescent and adult C57BL6/J mice of both sexes under the natural prey capture context compared to responses in our established virtual motion stimulus paradigm, C-SPOT. Most surprisingly, we discovered that female versus male adolescent mice have opposing innate behavioral biases evoked by the same sweeping motion stimuli which is not present in adulthood. Further, female mice display a robust enhancement of approach towards visual motion over all other groups tested, yet they are the least aggressive in response to live prey. Thus, our work overall revealed that innate approach towards visual motion is robustly dissociated from predatory aggression in female versus male mice specifically during adolescence. This underscores the different natural behavioral goals and physiological states that uniquely apply to female versus male adolescent animals, and reveals that approach towards visual motion is a key sensory-motor process selectively augmented during female adolescence. HighlightsO_LIAdolescent mice of both sexes innately approach insects more than adults C_LIO_LIAdolescent males versus females have distinct response biases to visual motion C_LIO_LIAdolescent males display the strongest hunger-related predatory aggression C_LI

animal behavior and cognition↗

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↗

Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse

The superior colliculus (SC) mediates rapid orienting to visual stimuli across species. To determine the specific circuits within the SC that drive orienting and approach behavior toward appetitive stimuli, we explored the role of three genetically defined cell types in mediating prey capture in mice. Chemogenetic inactivation of two classically defined cell types, the wide-field (WF) and narrow-field (NF) vertical neurons, revealed that they are involved in distinct aspects of prey capture. WF neurons were required for rapid prey detection and distant approach initiation, whereas NF neurons were required for continuous and accurate orienting during pursuit. In contrast, prey capture did not require parvalbumin-expressing (PV) neurons that have previously been implicated in fear responses. The visual coding of WF and NF cells in the awake mouse and their projection targets were consistent with their roles in prey detection versus pursuit. Thus, our studies link specific neural circuit connectivity and function with stimulus detection and orienting behavior, providing insight into visuomotor and attentional mechanisms mediated by superior colliculus.\n\nHighlightsO_LIThis study provides the first demonstration of the role of specific cell populations in the superior colliculus in orienting and approach behavior.\nC_LIO_LIA genetically targeted population of wide-field vertical neurons in the superior colliculus is required for rapid prey detection and initiation of long-distance approaches.\nC_LIO_LIA genetically targeted population of narrow-field vertical neurons is required for approach initiation, accurate targeting, and approach continuity.\nC_LIO_LIVisual response properties and projection targets of these cells are consistent with their role in prey capture, linking neural circuit connectivity and function with behavior.\nC_LI

neuroscience↗