An NMDA receptor-dependent mechanism for subcellular segregation of sensory inputs in the tadpole optic tectum

Hamodi, Ali S.; Liu, Zhenyu; Pratt, Kara G.

doi:10.7554/elife.20502

Cited by 10 publications

(12 citation statements)

References 64 publications

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“…Thus, acoustic stimulation tended to tune the network in the same direction as visual stimulation when delivered alone ( Figure 2D), but it negated the effects of visual stimulation when the two were combined. This effect is likely to be either a consequence of strong inhibitory recruitment during multisensory integration in the tectum Hamodi et al, 2016), or a sign of highly non-linear interactions between acoustic and visual inputs within the dendritic trees of individual tectal . Same data as in (C), shown as averages for each group, with 95% confidence intervals.…”

Section: Changes In Average Neuronal Tuning and Tuning Variabilitymentioning

confidence: 99%

Intrinsic temporal tuning of neurons in the optic tectum is shaped by multisensory experience

Busch

Khakhalin

2019

Preprint

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For a biological neural network to be functional, its neurons need to be connected with synapses of appropriate strength, and each neuron needs to appropriately respond to its synaptic inputs. This second aspect of network tuning is maintained by intrinsic plasticity; yet it is often considered secondary to changes in connectivity, and mostly limited to adjustments of overall excitability of each neuron. Here we argue that even non-oscillatory neurons can be tuned to inputs of different temporal dynamics, and that they can routinely adjust this tuning to match the statistics of their synaptic activation. Using the dynamic clamp technique, we show that in the tectum of Xenopus tadpoles, neurons become selective for faster inputs when animals are exposed to fast visual stimuli, but remain responsive to longer inputs in animals exposed to slower, looming or multisensory stimulation. We also report a homeostatic co-tuning between synaptic and intrinsic temporal properties of individual tectal cells. These results expand our understanding of intrinsic plasticity in the brain, and suggest that there may exist an additional dimension of network tuning that has been so far overlooked. 102(6):3392-3404. Richards, B. A. and Lillicrap, T. P. (2019). Dendritic solutions to the credit assignment problem. Current opinion in neurobiology, 54:28-36.

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Section: Changes In Average Neuronal Tuning and Tuning Variabilitymentioning

confidence: 99%

Intrinsic temporal tuning of neurons in the optic tectum is shaped by multisensory experience

Busch

Khakhalin

2019

Preprint

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“…In addition to visual input, tectal neurons receive input from several different non-visual sensory modalities including the auditory and lateral line systems (Hiramoto and Cline, 2009; Deeg et al, 2009; Hamodi et al, 2016), and local excitatory and inhibitory input from other tectal neurons. To determine if all excitatory synapses associated with PS-MO neurons were reduced, mEPSCs were recorded, and these data indicate a less pronounced decrease in current amplitude compared to that of the asEPSCs.…”

Section: Discussionmentioning

confidence: 99%

“…Nevertheless, given that weaker synapses are known to be less stable and have a higher probability of being lost than stronger ones (Ruthazer and Cline, 2006), the observed decrease in synapse number would be expected. In addition to visual input, tectal neurons receive input from several different non-visual sensory modalities including the auditory and lateral line systems (Deeg et al, 2009;Hiramoto and Cline, 2009;Hamodi et al, 2016), and local excitatory and inhibitory input from other tectal neurons. To determine if all excitatory synapses associated with PS-MO neurons were reduced, mEPSCs were recorded, and these data indicate a less pronounced decrease in current amplitude compared to that of the asEPSCs.…”

Section: Weaker and Fewer Retinotectal Synapses Recorded From Ps-mo Tmentioning

confidence: 99%

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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“…Synaptic competition attempted to keep close to a constant both the sum of synaptic inputs to each neuron, and the sum of outputs from each neuron. In practice, it means that every time a synapse connecting neurons i and j increased in strength, all output synapses of neuron i and all input synapses of neuron j were scaled down a bit (Cohen-Cory, 2002;Munz et al, 2014;Hamodi et al, 2016).…”

Section: Developmental Modelmentioning

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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An NMDA receptor-dependent mechanism for subcellular segregation of sensory inputs in the tadpole optic tectum

Cited by 10 publications

References 64 publications

Intrinsic temporal tuning of neurons in the optic tectum is shaped by multisensory experience

Intrinsic temporal tuning of neurons in the optic tectum is shaped by multisensory experience

Presenilin Regulates Retinotectal Synapse Formation through EphB2 Receptor Processing

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

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