Neuronal Dynamics Regulating Brain and Behavioral State Transitions

Andalman, Aaron S.; Burns, Vanessa M.; Lovett-Barron, Matthew; Broxton, Michael; Poole, Ben; Yang, Samuel J.; Grosenick, Logan; Lerner, Talia N.; Chen, Ritchie; Benster, Tyler; Mourrain, Philippe; Levoy, Marc; Rajan, Kanaka; Deisseroth, Karl

doi:10.1016/j.cell.2019.02.037

Cited by 212 publications

(276 citation statements)

References 95 publications

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“…In this study we investigated the functional development of habenular circuits across multiple developmental stages of zebrafish from relatively simpler larvae to juvenile zebrafish with complex behaviours (Amo et al, 2014;Andalman et al, 2019;Chou et al, 2016;Dreosti et al, 2015;Hinz and de Polavieja, 2017;Ksenia Yashina, 2019;Valente et al, 2012). The use of juvenile zebrafish is getting increasingly popular due to their transparent brains and expanded behavioural repertoire that requires habenular function (Andalman et al, 2019;Dreosti et al, 2015;Hinz and de Polavieja, 2017;Valente et al, 2012;Yashina et al, 2019). Our results revealed that as the zebrafish develop from larval to juvenile stage, habenular circuits undergo multiple transitions in its architecture, sensory computations and intrinsically generated spontaneous activity, which could support the expansion of the behavioural repertoire in developing zebrafish.…”

Section: Discussionmentioning

confidence: 99%

“…To study the functional development of zebrafish habenula, we focused on three developmental stages: 3dpf (early larval stage), 6dpf (late larval stage) and 21dpf (juvenile stage). During these periods, zebrafish transition from self-feeding larvae (via the yolk sac) to an external feeding juvenile animal with more complex behaviours including those involving habenular circuits (Agetsuma et al, 2010;Amo et al, 2014;Andalman et al, 2019;Dreosti et al, 2015;Hinz and de Polavieja, 2017;Valente et al, 2012). First, we visualized the gross morphology of Hb in Tg(elavl3:GCaMP6s) (Vladimirov et al, 2014) zebrafish, labelling most habenular neurons.…”

Section: New Neurons and New Inhibitory Connections Are Added To Habementioning

confidence: 99%

“…These results show for the first time that distinct functional clusters of spatially organized habenular neurons are born at a distinct developmental stage, and exhibit similar features of spontaneous activity. Accumulating evidence suggest that the distinct functional clusters of habenular neurons mediate distinct behaviours (Agetsuma et al, 2010;Amo et al, 2014;Andalman et al, 2019;Chou et al, 2016;Duboue et al, 2017;Lee et al, 2010). Sequential addition of new functional clusters with new properties across development could therefore explain the expansion of zebrafish behavioural repertoire across development (Dreosti et al, 2015;Valente et al, 2012).…”

Section: Temporal Features Of Spontaneous Habenular Activity Change Dmentioning

confidence: 99%

“…Two major subnuclei, the lateral and medial habenula in mammals, respectively dorsal habenula (dHb) and ventral habenula (vHb) in zebrafish, have clear differences in their functional and molecular profiles (Amo et al, 2014;Lee et al, 2010). While the dHb is involved in sensory processing Zhang et al, 2017), circadian rhythms , aggression (Chou et al, 2016) and experience dependent fear response (Agetsuma et al, 2010;Duboue et al, 2017;Lee et al, 2010), the vHb was shown to play a role in avoidance learning (Amo et al, 2014) and active coping behaviour (Andalman et al, 2019). In zebrafish, dHb and vHb originate from separate neural progenitor pools, and were suggested to maturate at distinct developmental time points (Beretta et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…In addition, spontaneous habenular activity was shown to govern sensory responses and therefore proposed to represent internal states of the network, which could mediate the selection of appropriate behaviours (Jetti et al, 2014). In fact, a recent study revealed a sequential recruitment of neurons generating an increase in vHb activity, during the switch from active to passive coping behaviours in juvenile zebrafish (Andalman et al, 2019). Interestingly, such complex behaviours emerge at later stages of zebrafish development (Dreosti et al, 2015;Hinz and de Polavieja, 2017;Valente et al, 2012;Yashina et al, 2019), suggesting pronounced changes in the underlying circuitry across the brain.…”

Section: Introductionmentioning

confidence: 99%

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Functional properties of habenular neurons are determined by developmental stage and sequential neurogenesis

Fore

Coşacak

Verdugo

et al. 2019

Preprint

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Neural development is not just a linear expansion of the brain. Instead, the structure and function of developing brain circuits undergo drastic alterations that have a direct impact on the animals' expanding behavioural repertoire. Here we investigated the developmental changes in the habenula, a brain region that mediates behavioural flexibility during learning, social interactions and aversive experiences. We showed that developing habenular circuits exhibit multiple alterations, which increase the structural and functional diversity of cell types, inputs and functional modules within habenula. As the neural architecture of habenula develops, it sequentially transforms into a multi-sensory brain region that can process visual and olfactory information. Moreover, we also observed that already at early developmental stages, the habenula exhibits spatio-temporally structured spontaneous neural activity that shows prominent alterations and refinement with age. Interestingly, these alterations in spontaneous activity are accompanied by sequential neurogenesis and integration of distinct neural clusters across development. Finally, by combining an in vivo neuronal birthdating method with functional imaging, we revealed that clusters of habenular neurons with distinct functional properties are born sequentially at distinct developmental time windows. Our results highlight a strong link between the function of habenular neurons and their precise birthdate during development, which supports the idea that sequential neurogenesis leads to an expansion of neural clusters that correspond to distinct functional modules in the brain.

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Section: Discussionmentioning

confidence: 99%

Section: New Neurons and New Inhibitory Connections Are Added To Habementioning

confidence: 99%

Section: Temporal Features Of Spontaneous Habenular Activity Change Dmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Functional properties of habenular neurons are determined by developmental stage and sequential neurogenesis

Fore

Coşacak

Verdugo

et al. 2019

Preprint

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Control of Brain State Transitions with a Photoswitchable Muscarinic Agonist

et al. 2021

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The ability to control neural activity is essential for research not only in basic neuroscience, as spatiotemporal control of activity is a fundamental experimental tool, but also in clinical neurology for therapeutic brain interventions. Transcranial-magnetic, ultrasound, and alternating/direct current (AC/DC) stimulation are some available means of spatiotemporal controlled neuromodulation. There is also light-mediated control, such as optogenetics, which has revolutionized neuroscience research, yet its clinical translation is hampered by the need for gene manipulation. As a drug-based light-mediated control, the effect of a photoswitchable muscarinic agonist (Phthalimide-Azo-Iper (PAI)) on a brain network is evaluated in this study. First, the conditions to manipulate M2 muscarinic receptors with light in the experimental setup are determined. Next, physiological synchronous emergent cortical activity consisting of slow oscillations-as in slow wave sleep-is transformed into a higher frequency pattern in the cerebral cortex, both in vitro and in vivo, as a consequence of PAI activation with light. These results open the way to study cholinergic neuromodulation and to control spatiotemporal patterns of activity in different brain states, their transitions, and their links to cognition and behavior. The approach can be applied to different organisms and does not require genetic manipulation, which would make it translational to humans.

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Memristor‐Based Intelligent Human‐Like Neural Computing

Wang

Song

Chen

et al. 2022

Adv Elect Materials

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In the field of a relatively dangerous working environment, NASA developed Valkyrie, a 44-degree-of-freedom, series elastic actuator-based robot. In addition, Valkyrie is designed to respond to disasters like nuclear disasters and advance human spaceflight in extraterrestrial planetary settings. [6] By implementing safety features and allowing remote intervention, Atkeson et al. enabled an Atlas humanoid robot to meet the standard in performing disaster response-related tasks involving physical contact with the environment. [7] Currently, to allow humanoid robots to feel and process the environmental information as human beings for perfectly implementing tasks, perceptual comprehension and computation efficiency are two key indexes. Nevertheless, it is challenging to achieve them. The former requires the installation of massive, diverse sensors in humanoids, which will inevitably slow down the processing speed under the current sensing-storage-process separated framework, i.e., von Neumann architecture. In other words, the current computer architecture builds up a barrier between sensing performance and computation efficiency. In this context, neuromorphic devices which can emulate the perceptual and computation functions of the biological nervous system have illustrated their potential to break the von Neumann barrier, attracting researchers' interests (Figure 1). Humanoid robots, intelligent machines resembling the human body in shape and functions, cannot only replace humans to complete services and dangerous tasks but also deepen the own understanding of the human body in the mimicking process. Nowadays, attaching a large number of sensors to obtain more sensory information and efficient computation is the development trend for humanoid robots. Nevertheless, due to the constraints of von Neumann-based structures, humanoid robots are facing multiple challenges, including tremendous energy consumption, latency bottlenecks, and the lack of bionic properties. Memristors, featured with high similarity to the biological elements, play an important role in mimicking the biological nervous system. The memristor-based nervous system allows humanoid robots to obtain high energy efficiency and bionic sensing properties, which are similar properties to the biological nervous system. Herein, this article first reviews the biological nervous system and memristor-based nervous system thoroughly, including the structures and also the functions. The applications of memristor-based nervous systems are introduced, the difficulties that need to be overcome are put forward, and future development prospects are also discussed. This review can hopefully provide an evolutionary perspective on humanoid robots and memristor-based nervous systems.

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Neuronal Dynamics Regulating Brain and Behavioral State Transitions

Cited by 212 publications

References 95 publications

Functional properties of habenular neurons are determined by developmental stage and sequential neurogenesis

Functional properties of habenular neurons are determined by developmental stage and sequential neurogenesis

Control of Brain State Transitions with a Photoswitchable Muscarinic Agonist

Memristor‐Based Intelligent Human‐Like Neural Computing

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