Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish

Animals from insects to humans perform visual escape behavior in response to looming stimuli, and these responses habituate if looms are presented repeatedly without consequence. While the basic visual processing and motor pathways involved in this behavior have been described, many of the nuances of predator perception and sensorimotor gating have not. Here, we have performed both behavioral analyses and brain-wide cellular-resolution calcium imaging in larval zebrafish while presenting them with visual loom stimuli or stimuli that selectively deliver either the movement or the dimming properties of full loom stimuli. Behaviorally, we find that, while responses to repeated loom stimuli habituate, no such habituation occurs when repeated movement stimuli (in the absence of luminance changes) are presented. Dim stimuli seldom elicit escape responses, and therefore cannot habituate. Neither repeated movement stimuli nor repeated dimming stimuli habituate the responses to subsequent full loom stimuli, suggesting that full looms are required for habituation. Our calcium imaging reveals that motion-sensitive neurons are abundant in the brain, that dim-sensitive neurons are present but more rare, and that neurons responsive to both stimuli (and to full loom stimuli) are concentrated in the tectum. Neurons selective to full loom stimuli (but not to movement or dimming) were not evident. Finally, we explored whether movement- or dim-sensitive neurons have characteristic response profiles during habituation to full looms. Such functional links between baseline responsiveness and habituation rate could suggest a specific role in the brain-wide habituation network, but no such relationships were found in our data. Overall, our results suggest that, while both movement- and dim-sensitive neurons contribute to predator escape behavior, neither plays a specific role in brain-wide visual habituation networks or in behavioral habituation.

Dysfunctions in Infants’ Statistical Learning are Related to Parental Autistic Traits

Statistical learning refers to the ability to extract the statistical relations embedded in a sequence, and it plays a crucial role in the development of communicative and social skills that are impacted in the Autism Spectrum Disorder (ASD). Here, we investigated the relationship between infants’ SL ability and autistic traits in their parents. Using a visual habituation task, we tested infant offspring of adults (non-diagnosed) who show high (HAT infants) versus low (LAT infants) autistic traits. Results demonstrated that LAT infants learned the statistical structure embedded in a visual sequence, while HAT infants failed. Moreover, infants’ SL ability was related to autistic traits in their parents, further suggesting that early dysfunctions in SL might contribute to variabilities in ASD symptoms.

Brain-wide visual habituation networks in wild type and fmr1 zebrafish

Habituation is a form of learning during which animals stop responding to repetitive stimuli, and deficits in habituation are characteristics of several psychiatric disorders. Due to the technical challenges of measuring brain activity comprehensively and at cellular resolution, the brain-wide networks mediating habituation are poorly understood. Here we report brain-wide calcium imaging during visual learning in larval zebrafish as they habituate to repeated threatening loom stimuli. We show that different functional categories of loom-sensitive neurons are located in characteristic locations throughout the brain, and that both the functional properties of their networks and the resulting behavior can be modulated by stimulus saliency and timing. Using graph theory, we identify a principally visual circuit that habituates minimally, a moderately habituating midbrain population proposed to mediate the sensorimotor transformation, and downstream circuit elements responsible for higher order representations and the delivery of behavior. Zebrafish larvae carrying a mutation in the fmr1 gene have a systematic shift towards sustained premotor activity in this network, and show slower behavioral habituation. This represents the first description of a visual learning network across the brain at cellular resolution, and provides insights into the circuit-level changes that may occur in people with Fragile X syndrome and related psychiatric conditions.

An increase in spontaneous activity mediates visual habituation

The cerebral cortex is spontaneously active, but the function of this ongoing activity remains unclear. One possibility is that spontaneous activity provides contextual information in cortical computations, replaying previously learned patterns of activity that conditions the cortex to respond more efficiently, based on past experience. To test this, we measured the response of neuronal populations in mouse primary visual cortex with chronic two-photon calcium imaging during a visual habituation to a specific oriented stimulus. We unexpectedly found that, during habituation, spontaneous activity increased in neurons across the full range of orientation selectivity, eventually matching that of evoked levels. The increase in spontaneous activity strongly correlated with the degree of habituation. In fact, boosting spontaneous activity with two-photon optogenetic stimulation to the levels of stimulus-evoked activity induced habituation in naive animals. Our study shows that cortical spontaneous activity is causally linked to habituation, which unfolds by minimizing the difference between spontaneous and stimulus-evoked activity levels, rendering the cortex less responsive. We also show how manipulating spontaneous activity can accelerate this type of learning. We hypothesize that spontaneous activity in visual cortex gates incoming sensory information.

Distributed plasticity drives visual habituation learning in larval zebrafish

Habituation is a simple form of learning, where animals learn to reduce their responses to repeated innocuous stimuli. While habituation is simple in concept, its exact implementation in the vertebrate brain is not clear. It could occur via a single plasticity event at a singular site in the circuit, or alternatively via more complex strategies that combine multiple mechanisms at various processing stages and sites. Here, we use a visual habituation assay in larval zebrafish, where larvae habituate to sudden reductions in illumination (dark flashes). We find that 8 different components of this response habituate, including the probability of executing a response, its latency, and measures of its magnitude. Through behavioural analyses, we find that habituation of these different behavioural components occurs independently of each other and at different locations in the circuit. Further, we use genetic and pharmacological manipulations to show that habituation of different behavioural components are molecularly distinct. These results are consistent with a model by which visual habituation originates from the combination of multiple independent processes, which each act to adapt specific components of behaviour. This may allow animals to more specifically habituate behaviour based on stimulus context or internal state.

No perceptual reorganization for Limburgian tones? A cross-linguistic investigation with 6- to 12-month-old infants

Despite the fact that many of the world's languages use lexical tone, the majority of language acquisition studies has focused on non-tone languages. Research on tone languages has typically investigated well-known tone languages such as Mandarin and Cantonese Chinese. The current study looked at a Limburgian dialect of Dutch that uses lexical pitch differences, albeit in a rather restricted way. Using a visual habituation paradigm, 6- to 12-month-old Limburgian and Dutch infants were tested for their ability to discriminate Limburgian tones. The results showed that both Limburgian and Dutch infants discriminate the Limburgian tones throughout their first year of life. The role of linguistic experience, acoustic salience, and the degree of similarity to the native prosodic system are discussed.