A population of gap junction-coupled neurons drives recurrent network activity in a developing visual circuit

Liu, Zhenyu; Ciarleglio, Christopher M.; Hamodi, Ali S.; Aizenman, Carlos D.; Pratt, Kara G.

doi:10.1152/jn.01046.2015

Cited by 7 publications

(10 citation statements)

References 37 publications

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“…This finding suggests that developing tectal networks in Xenopus tadpoles may employ a yet undescribed homeostatic mechanism to balance relative abundance and strength of direct and recurrent synaptic connections in principal tectal cells, keeping it in the range that supports collision avoidance computations. Our modeling data also suggests that collision detection may be further improved by recurrent feedback inhibition (Khakhalin et al, 2014; Liu et al, 2016), especially for networks that are tightly connected and susceptible to epileptiform activity, or when the level of spontaneous neuronal noise in the system is high. We hypothesize that delayed feedback inhibition may act as a safeguard, temporally limiting recurrent activity in the network, and thus allowing for strong integration between direct and recurrent inputs within the window before the inhibition onset, without the risk of succumbing to epileptiform activity.…”

Section: Discussionmentioning

confidence: 61%

“…As the topology of recurrent connections in the tadpole tectum is not known (Pratt et al, 2008; Liu et al, 2016), we considered three possible configurations (Figure 2B): uniform , with random connections across the entire network and uniformly distributed connection weights; local , with connections spanning 5 nearby cells in each direction, and with average strength decreasing with distance; and scale-free : a small-world network with a few strongly connected hub cells linking the entire network in a set of connected clusters (Barabasi and Albert, 1999). All connectivity profiles were normalized by synaptic strength, so that the average sum of synaptic inputs received by tectal cells was same in each network type, regardless of its topology.…”

Section: Resultsmentioning

confidence: 99%

“…It is known that principal neurons in the tectum receive strong recurrent excitation (Pratt et al, 2008; Liu et al, 2016) that supports spontaneous neuronal activity during development (Pratt and Aizenman, 2007; Imaizumi et al, 2013; James et al, 2015). Principal tectal neurons also demonstrate prominent and rapid inactivation of spiking (Aizenman et al, 2003; Ciarleglio et al, 2015), which allowed us to suggest that together these two phenomena may underlie, or at least contribute to collision detection (Khakhalin et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…How then does a developing nervous system balance the need to sustain spontaneous activity with the ability to effectively process and react to external sensory stimuli? Here we examine the process of collision detection in Xenopus laevis tadpole tectum, in which activity generated through recurrent connectivity (Pratt et al, 2008; Liu et al, 2016) can interact with waves of evoked visual responses, potentially leading to differential reactions to different visual stimuli (Khakhalin et al, 2014). …”

Section: Introductionmentioning

confidence: 99%

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Emergence of Selectivity to Looming Stimuli in a Spiking Network Model of the Optic Tectum

Jang

Ramirez-Vizcarrondo

Aizenman

et al. 2016

Front. Neural Circuits

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The neural circuits in the optic tectum of Xenopus tadpoles are selectively responsive to looming visual stimuli that resemble objects approaching the animal at a collision trajectory. This selectivity is required for adaptive collision avoidance behavior in this species, but its underlying mechanisms are not known. In particular, it is still unclear how the balance between the recurrent spontaneous network activity and the newly arriving sensory flow is set in this structure, and to what degree this balance is important for collision detection. Also, despite the clear indication for the presence of strong recurrent excitation and spontaneous activity, the exact topology of recurrent feedback circuits in the tectum remains elusive. In this study we take advantage of recently published detailed cell-level data from tadpole tectum to build an informed computational model of it, and investigate whether dynamic activation in excitatory recurrent retinotopic networks may on its own underlie collision detection. We consider several possible recurrent connectivity configurations and compare their performance for collision detection under different levels of spontaneous neural activity. We show that even in the absence of inhibition, a retinotopic network of quickly inactivating spiking neurons is naturally selective for looming stimuli, but this selectivity is not robust to neuronal noise, and is sensitive to the balance between direct and recurrent inputs. We also describe how homeostatic modulation of intrinsic properties of individual tectal cells can change selectivity thresholds in this network, and qualitatively verify our predictions in a behavioral experiment in freely swimming tadpoles.

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Section: Discussionmentioning

confidence: 61%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Emergence of Selectivity to Looming Stimuli in a Spiking Network Model of the Optic Tectum

Jang

Ramirez-Vizcarrondo

Aizenman

et al. 2016

Front. Neural Circuits

Self Cite

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“…Contrary to our expectations, and in contrast to what is known about visual inputs to the tectum (Tao and Poo, 2005), the intra-tectal connectivity did not become more compact in development (p t =0.7). This suggests that tectal networks rely on relatively far-reaching recurrent connections to integrate visual information across the visual field (Baginskas and Kuras, 2009;Liu et al, 2016;Jang et al, 2016). A.…”

Section: Network Reconstructionmentioning

confidence: 99%

Graph analysis of looming-selective networks in the tectum, and its replication in a simple computational model

Khakhalin

2019

Preprint

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Looming stimuli evoke behavioral responses in most sighted animals, yet the mechanisms of looming detection in vertebrates are poorly understood. Here we hypothesize that looming detection in the tectum may rely on spontaneous emergence of synfire chains: groups of neurons connected to each other in the same sequence in which they are activated during a loom. We then test some specific consequences of this hypothesis. First, we use high-speed calcium imaging to reconstruct connectivity of small networks within the tectum of Xenopus tadpoles. We report that reconstructed directed graphs are clustered and hierarchical, that their modularity increases in development, and that looming-selective cells tend to act as activation sinks within these graphs. Second, we describe spontaneous emergence of looming selectivity in a computational developmental model of the tectum, governed by both synaptic and intrinsic plasticity, and driven by structured visual inputs. We show that synfire chains contribute to looming detection in the model; that structured inputs are critical for the emergence of selectivity, and that biological tectal networks follow most, but not all predictions of the model. Finally, we propose a conceptual scheme for understanding the emergence and fine-tuning of collision detection in developing aquatic animals. 14(4):505.

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Presenilin Regulates Retinotectal Synapse Formation through EphB2 Receptor Processing

Liu

Thakar

Santoro

et al. 2018

Developmental Neurobiology

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As the catalytic component of γ-secretase, presenilin (PS) has long been studied in the context of Alzheimer’s disease through cleaving the amyloid precursor protein. PS/γ-secretase, however, also cleaves a multitude of single-pass transmembrane proteins that are important during development, including Notch, the netrin receptor DCC, cadherins, drebrin-A, and the EphB2 receptor. Because transgenic PS-KO mice do not survive to birth, studies of this molecule during later embryonic or early postnatal stages of development have been carried out using cell cultures or conditional knock-out mice, respectively. As a result, the function of PS in synapse formation had not been well-addressed. Here we study the role of PS in the developing Xenopus tadpole retinotectal circuit, an in-vivo model that allows for protein expression to be manipulated specifically during the peak of synapse formation between retinal ganglion cells and tectal neurons. We found that inhibiting PS in the postsynaptic tectal neurons impaired tadpole visual avoidance behavior. Whole cell recordings indicated weaker retinotectal synaptic transmission which was characterized by significant reductions in both NMDA receptor (NMDAR)- and AMPA receptor (AMPAR)-mediated currents. We also found that expression of the C-tail fragment of the EphB2 receptor, which is normally cleaved by PS/γ-secretase and which has been shown to upregulate NMDARs at the synapse, rescued the reduced NMDAR-mediated responses. Our data determine that normal PS function is important for proper formation and strengthening of retinotectal synapses through cleaving the EphB2 receptor.

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A population of gap junction-coupled neurons drives recurrent network activity in a developing visual circuit

Abstract: Liu Z, Ciarleglio CM, Hamodi AS, Aizenman CD, Pratt KG. A population of gap junction-coupled neurons drives recurrent network activity in a developing visual circuit.

Cited by 7 publications

References 37 publications

Emergence of Selectivity to Looming Stimuli in a Spiking Network Model of the Optic Tectum

Emergence of Selectivity to Looming Stimuli in a Spiking Network Model of the Optic Tectum

Graph analysis of looming-selective networks in the tectum, and its replication in a simple computational model

Presenilin Regulates Retinotectal Synapse Formation through EphB2 Receptor Processing

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