The development of synaptic transmission is time-locked to early social behaviors in rats

Naskar, Shovan; Narducci, Roberto; Balzani, Edoardo; Cwetsch, Andrzej; Tucci, Valter; Cancedda, Laura

doi:10.1038/s41467-019-09156-3

Cited by 41 publications

(42 citation statements)

References 51 publications

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“…We tested the specificity of our construct through immunohistochemistry for somatostatin: 83 ± 8% of cells expressing the inhibitory hM4Di-DREADD also expressed somatostatin (n = 4 animals, Fig 5B) and 79 ± 6% of SST cells expressed the hM4Di-DREADD. We also confirmed that at this age, activation of the hM4Di-DREADD construct with clozapine reduced excitability of DREADD-expressing cells in vitro ( Supplementary Fig 2A) similar to the excitability reducing effect of hM4Di-DREADD activation in developing layer 2/3 pyramidal neurons described previously (Naskar et al, 2019).…”

Section: Somatostatin Cell Suppression Reduce Event Specificitysupporting

confidence: 90%

Control of spontaneous activity patterns by inhibitory signaling in the developing visual cortex

Leighton

Houwen

Cheyne

et al. 2020

Preprint

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During early development, even before the senses are active, bursts of activity travel across the nervous system. This spontaneously generated activity drives the refinement of synaptic connections, preparing young networks for patterned sensory input. Synaptic fine-tuning relies not only on the presence of spontaneous activity, but also on the specific characteristics of these activity patterns, such as their frequency, amplitude and synchronicity. Here, we provide evidence that these crucial characteristics are shaped by the relative balance of excitation and inhibition, where patterns with distinct characteristics have different excitatory/inhibitory ratios. Inhibition can control whether cells participate during a spontaneous event, as pharmacogenetic suppression of the somatostatin (SST) expressing subtype of inhibitory interneurons increased cell recruitment and lateral spread of events. KeywordsMouse, in vivo, pharmacogenetics, somatostatin expressing interneuron, VIP expressing interneuron, calcium imaging, DREADD

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Section: Somatostatin Cell Suppression Reduce Event Specificitysupporting

confidence: 90%

Control of spontaneous activity patterns by inhibitory signaling in the developing visual cortex

Leighton

Houwen

Cheyne

et al. 2020

Preprint

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“…We specifically inactivated SST + interneurons by using a Cre-dependent inhibitory DREADD delivered by virus injections, which results in 80% of the SST + interneurons expressing the hM4Di-DREADD construct 28 . Bath application of clozapine in vitro reduced the excitability of SST + interneurons 28 , replicating previous findings that hM4Di-DREADD activation reduces the excitability of developing layer 2/3 neurons 36 . We performed in vivo wide-field calcium imaging to monitor spontaneous network activity in V1 and then activated the iDREADD receptor by injecting clozapine subcutaneously (Fig.…”

Section: Oxytocin Modulates Spontaneous Activity Patterns Activatingsupporting

confidence: 87%

Oxytocin shapes spontaneous activity patterns in the developing visual cortex by activating somatostatin interneurons

Maldonado

Nuno-Perez

Kirchner

et al. 2019

Preprint

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Spontaneous network activity shapes emerging neuronal circuits during early brain development, however how neuromodulation influences this activity is not fully understood.Here, we report that the neuromodulator oxytocin powerfully shapes spontaneous activity patterns. In vivo, oxytocin strongly decreased the frequency and pairwise correlations of spontaneous activity events in visual cortex (V1), but not in somatosensory cortex (S1). This differential effect was a consequence of oxytocin only increasing inhibition in V1 and increasing both inhibition and excitation in S1. The increase in inhibition was mediated by the depolarization and increase in excitability of somatostatin + (SST) interneurons specifically.Accordingly, silencing SST + neurons pharmacogenetically fully blocked oxytocin's effect on inhibition in vitro as well its effect on spontaneous activity patterns in vivo. Thus, oxytocin decreases the excitatory/inhibitory ratio and modulates specific features of V1 spontaneous activity patterns that are crucial for refining developing synaptic connections and sensory processing later in life.We observed spontaneous network activity in V1, S1 and higher visual areas (Fig. 1a, b).Frequently, network events were confined to individual sensory regions, but sometimes occurred across the entire field of view. After topical application of oxytocin (1 µM) onto the cortical surface, the occurrence of network events was strongly decreased in V1, but only

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“…Also, pyramidal cells in the mouse and ferret visual cortex are already orientation selective at (43) and before (44,45) eye opening, providing another likely source of the synaptic Gabor receptive fields in our model. We find that a rapid increase in spine density during the second postnatal week (60) , which possibly indicates the establishment of dense, intralaminar and intercortical connections (61) , does not disrupt already established synaptic clusters ( Supplementary Fig. 16).…”

Section: Discussionmentioning

confidence: 83%

“…This novel synapse could potentially come from a pool of silent synapses, a type of synapse that lacks AMPA receptors but can become unsilenced through activity-dependent mechanisms (80) . While we maintain a constant density of synapses throughout our simulations, a rapid increase in synaptic density like the one observed during development in the somatosensory cortex (61) does not interfere with the formation of synaptic clustering ( Supplementary Fig. 16).…”

Section: Retinal Wave Generationmentioning

confidence: 95%

A unifying framework for synaptic organization on cortical dendrites

Kirchner

Gjorgjieva

2019

Preprint

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Dendritic synaptic inputs are organized into functional clusters with remarkable subcellular precision at the micron level. This organization emerges during early postnatal development through patterned spontaneous activity and manifests both locally where nearby synapses are significantly correlated, and globally with distance to the soma. We propose a biophysically motivated synaptic plasticity model to dissect the mechanistic origins of this organization during development, and elucidate synaptic clustering of different stimulus features in the adult. Our model captures local clustering of orientation in ferret vs. receptive field overlap in mouse visual cortex based on the cortical magnification of visual space. Including a back-propagating action potential explains branch clustering heterogeneity in the ferret, and produces a global retinotopy gradient from soma to dendrite in the mouse. Therefore, our framework suggests that sub-cellular precision in connectivity can already be established in development, and unifies different aspects of synaptic organization across species and scales.Neurons in the developing brain are already precisely connected before sensory organs mature. It is widely accepted that spontaneous activity refines circuit connectivity to mature levels at the scale of single neurons and networks. Recent studies have revealed that spontaneous activity can also establish fine-scale organization of individual synapses within the dendritic arborizations of single neurons (1,2) . One striking example of this organization is functional synaptic clustering: synapses onto dendrites of pyramidal neurons that receive correlated input or encode a common sensory feature are spatially grouped. Synaptic clustering has been observed across brain regions, developmental ages and diverse species from rodent to primate (1-10) and has multiple functional benefits; it compartmentalizes the dendrites of single neurons, enables supra-linear integration of inputs and shapes memory

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The development of synaptic transmission is time-locked to early social behaviors in rats

Cited by 41 publications

References 51 publications

Control of spontaneous activity patterns by inhibitory signaling in the developing visual cortex

Control of spontaneous activity patterns by inhibitory signaling in the developing visual cortex

Oxytocin shapes spontaneous activity patterns in the developing visual cortex by activating somatostatin interneurons

A unifying framework for synaptic organization on cortical dendrites

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