Left Habenula Mediates Light-Preference Behavior in Zebrafish via an Asymmetrical Visual Pathway

Zhang, Baibing; Yao, Yuanyuan; Zhang, Hefei; Kikuchi, Kôichi; Du, Jiulin

doi:10.1016/j.neuron.2017.01.011

Cited by 97 publications

(153 citation statements)

References 67 publications

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“…Larvae were then returned to E3 medium. Survival was comparable to that of non-enucleated controls (> 95%) confirming previous reports in which development of the larva was no affected by single-eye enucleations [52, 54, 55, 56]. …”

Section: Methodssupporting

confidence: 87%

Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits

et al. 2017

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SummaryFrom development up to adulthood, the vertebrate brain is continuously supplied with newborn neurons that integrate into established mature circuits. However, how this process is coordinated during development remains unclear. Using two-photon imaging, GCaMP5 transgenic zebrafish larvae, and sparse electroporation in the larva’s optic tectum, we monitored spontaneous and induced activity of large neuronal populations containing newborn and functionally mature neurons. We observed that the maturation of newborn neurons is a 4-day process. Initially, newborn neurons showed undeveloped dendritic arbors, no neurotransmitter identity, and were unresponsive to visual stimulation, although they displayed spontaneous calcium transients. Later on, newborn-labeled neurons began to respond to visual stimuli but in a very variable manner. At the end of the maturation period, newborn-labeled neurons exhibited visual tuning curves (spatial receptive fields and direction selectivity) and spontaneous correlated activity with neighboring functionally mature neurons. At this developmental stage, newborn-labeled neurons presented complex dendritic arbors and neurotransmitter identity (excitatory or inhibitory). Removal of retinal inputs significantly perturbed the integration of newborn neurons into the functionally mature tectal network. Our results provide a comprehensive description of the maturation of newborn neurons during development and shed light on potential mechanisms underlying their integration into a functionally mature neuronal circuit.

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Section: Methodssupporting

confidence: 87%

Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits

et al. 2017

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“…Connectivity from this nucleus to the habenula has been shown by several groups 24, 28, 29 . The neuropil of the nucleus rostrolateralis may include the arborization field AF4 24, 30 .…”

Section: Discussionmentioning

confidence: 83%

“…This was confirmed recently by Zhang et al . 29 , who showed that retinal ganglion cells innervating AF4 expressing opn4xa .…”

Section: Discussionmentioning

confidence: 99%

Masking of a circadian behavior in larval zebrafish involves the thalamo-habenula pathway

Lin

Jesuthasan

2017

Sci Rep

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Changes in illumination can rapidly influence behavior that is normally controlled by the circadian clock. This effect is termed masking. In mice, masking requires melanopsin-expressing retinal ganglion cells that detect blue light and project to the thalamus. It is not known whether masking is wavelength-dependent in other vertebrates, nor is it known whether the thalamus is also involved or how it influences masking. Here, we address these questions in zebrafish. We find that diel vertical migration, a circadian behavior in larval zebrafish, is effectively triggered by blue, but not by red light. Two-photon calcium imaging reveals that a thalamic nucleus and a downstream structure, the habenula, have a sustained response to blue but not to red light. Lesioning the habenula reduces light-evoked climbing. These data suggest that the thalamo-habenula pathway is involved in the ability of blue light to influence a circadian behavior.

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“…The left dHb was recently shown to receive visual input from a specific type of retinal ganglion cell via EmT afferent connections [26]. In agreement with these differences in connectivity, the left and right dHb differentially respond to light and odor cues [26–28]. Since only 20% of left dHb neurons are light-responsive [27], most likely they comprise a distinct set than those that attenuate fear.…”

Section: Discussionmentioning

confidence: 94%

“…Notably, axons from a bilaterally distributed subset of olfactory mitral cells terminate in a discrete region of only the right dHb [25]. The left dHb was recently shown to receive visual input from a specific type of retinal ganglion cell via EmT afferent connections [26]. In agreement with these differences in connectivity, the left and right dHb differentially respond to light and odor cues [26–28].…”

Section: Discussionmentioning

confidence: 99%

Left Habenular Activity Attenuates Fear Responses in Larval Zebrafish

et al. 2017

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Summary Fear responses are defensive states that ensure survival of an organism in the presence of a threat. Perception of an aversive cue causes changes in behavior and physiology, such as freezing and elevated cortisol, followed by a return to the baseline state when the threat is evaded [1]. Neural systems that elicit fear behaviors include the amygdala, hippocampus and medial prefrontal cortex. However, aside from a few examples, little is known about brain regions that promote recovery from an aversive event [2]. Previous studies had implicated the dorsal habenular nuclei in regulating fear responses and boldness in zebrafish [3–7]. We now show that perturbation of the inherent left-right (L-R) asymmetry of the dorsal habenulo-interpeduncular (dHb-IPN) pathway at larval stages expedites the return of locomotor activity following an unexpected negative stimulus, electric shock. Severing habenular efferents to the IPN, or only those from the left dHb, prolongs the freezing behavior that follows shock. Individuals with symmetric, right isomerized dHb also exhibit increased freezing. In contrast, larvae that have symmetric, left-isomerized dHb, or in which just the left dHb-IPN projection is optogenetically activated, rapidly resume swimming post shock. In vivo calcium imaging reveals a neuronal subset, predominantly in the left dHb, whose activation is correlated with resumption of swimming. The results demonstrate functional specialization of the left dHb-IPN pathway in attenuating the response to fear.

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Left Habenula Mediates Light-Preference Behavior in Zebrafish via an Asymmetrical Visual Pathway

Cited by 97 publications

References 67 publications

Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits

Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits

Masking of a circadian behavior in larval zebrafish involves the thalamo-habenula pathway

Left Habenular Activity Attenuates Fear Responses in Larval Zebrafish

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