Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum

Peng, Yangfan; Tomás, Federico José Barreda; Klisch, Constantin; Vida, Imre; Geiger, Jörg R. P.

doi:10.1093/cercor/bhx049

Cited by 47 publications

(91 citation statements)

References 83 publications

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“…The inter-soma distances were not correlated with the connection probability (Figure 4). This result appears similar to the previously reported spatial patterns of CA3 connectivity (Guzman et al, 2016) but is different from those of neocortical connectivity, in which more adjacent pairs had a higher probability of connections (Peng et al, 2017; Perin et al, 2011; Song et al, 2005). When considering the connectivity, however, one needs to consider the anatomical size of the CA2 region; the majority of CA2 cell pairs have inter-soma distances of less than 100 µm; thus, we cannot rule out the possibility that this sampling restriction masked the distance dependence.…”

Section: Resultssupporting

confidence: 84%

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Recurrent connections between CA2 pyramidal cells

Okamoto

Ikegaya

2018

Preprint

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0Recurrent excitatory synapses are shown theoretically to play roles in memory storage 2 1 and associative learning, and such recurrent synapses are well described to occur in the 2 2 CA3 region of the hippocampus. Here, we report that the CA2 region also contains pairs. These connected pairs were located preferentially in the superficial layer and circuits are dense in the CA2 region as well as in the CA3 region. All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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Section: Resultssupporting

confidence: 84%

“…The CA3 network contains clustered circuit motifs (Guzman et al, 2016). The neocortex also contains rich clustered connections (Peng et al, 2017; Perin et al, 2011; Song et al, 2005). In CA2 pyramidal cells, we did not find bidirectionally connected pairs.…”

Section: Resultsmentioning

confidence: 99%

Recurrent connections between CA2 pyramidal cells

Okamoto

Ikegaya

2018

Preprint

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“…Increasing the number of pipettes per trial helps test more possible connections giving the opportunity to look at higher order connectivity motifs (Guzman et al, 2016; Peng et al, 2017) and provides the experimenter with a higher chance of obtaining a dual recording. While we have successfully used 4 pipettes to obtain quadruple whole-cell recordings ( Figure 2A-E ), our data on success rates ( Figure 2G-H ) was taken from a series of experiments using 3 pipettes.…”

Section: Discussionmentioning

confidence: 99%

“…Both in vitro and in vivo studies are normally made blind to connectivity which can lead to many frustrating recordings from unconnected pairs of neurons. One way to address this is to increase the numbers of recording pipettes to allow the testing of more connections per recording session (Peng et al, 2017; Perin et al, 2011). Another could be to use transsynaptic tracing to visulaise connected pairs of neurons prior to recording (Wickersham et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Multiple two-photon targeted whole-cell patch-clamp recordings from monosynaptically connected neurons in vivo

Jouhanneau

Poulet

2019

Preprint

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28Although we know a great deal about monosynaptic connectivity, transmission and integration 29 in the mammalian nervous system from in vitro studies, very little is known in vivo. This is partly 30 because it is technically difficult to evoke action potentials and simultaneously record small 31 amplitude subthreshold responses in closely (< 150 µm) located pairs of neurons. To address 32 this, we have developed in vivo two-photon targeted multiple (2 -4) whole-cell patch clamp 33 recordings of nearby neurons in superficial layers 1 to 3 of primary somatosensory cortex. 34Here we describe a step-by-step guide to this approach in the anesthetised mouse, including: 35 the design of the setup, surgery, preparation of pipettes, targeting and acquisition of multiple 36 whole-cell recordings, as well as in vivo and post-hoc histology. The procedure takes ~ 4 hours 37 from start of surgery to end of recording and allows examinations both into the 38 electrophysiological features of unitary excitatory and inhibitory monosynaptic inputs and the 39 synaptic mechanisms of correlated neuronal activity.45 properties of synapses. In the intact brain, however, synapses function during different 46 behavioural and network states as well fluctuating levels of neuromodulators and far less is 47 known about monosynaptic transmission and the activity of connected neurons in vivo. 48In vivo approaches to identify connected pairs of neurons in the mammalian nervous system 49 have typically performed electrophysiological recordings of multiple single neurons and 50 examined the average response of one neuron to spontaneously occurring action potentials in 51 another neuron. "Spike triggered averaging" of cortical neurons has been performed both with 52 multiple extracellular recordings (Bartho, 2004; Csicsvari et al., 1998; English et al., 2017; 53 Fujisawa et al., 2008; Reid and Alonso, 1995; Swadlow and Gusev, 2002) and a combination 54 of extracellular and intracellular membrane potential recordings (Bruno, 2006; Crochet et al., 55 2005; London et al., 2010; Matsumura et al., 1996; Yu and Ferster, 2013). However, because 56 it is not yet possible to record the activity of all neurons presynaptic to the cells of interest and 57 cortical neurons can fire simultaneously, it is difficult to confirm whether correlated activity is 58 the result of a direct synaptic connection between the two recorded neurons or input from a 59 third, unrecorded, neuron with similar firing dynamics. One approach to get around the problem 60 of synchronous input is to have experimental control of action potential timing using single cell 61 stimulation, while simultaneously recording the evoked membrane potential response from a 62 second neuron. While, care has to be taken in concluding that any synaptic response is the 63 result of a monosynaptic rather than polysynaptic input (Berry and Pentreath, 1976; Parker, 64 2010), this approach has been used in vivo to characterise the wiring and functional properties

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“…Recent work has revealed some properties of circuits involving presubicular principal cells and interneurons (Nassar et al, 2015;Simonnet et al, 2013;Peng et al, 2017). Local interactions between pyramidal cells and Somatostatin (SST) expressing Martinotti cells may help sustain firing in head direction cells .…”

Section: Introductionmentioning

confidence: 99%

Anterior thalamic excitation and feed-forward inhibition of presubicular neurons projecting to medial entorhinal cortex

Nassar

Simonnet

Huang

et al. 2018

Preprint

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The presubiculum contains head direction cells that are crucial for spatial navigation. Here, we examined the connectivity and strengths of thalamic inputs to presubicular layer 3 neurons projecting to the medial entorhinal cortex in the mouse. We recorded pairs of projection neurons and interneurons while optogenetically stimulating afferent fibers from the anterior thalamic nuclei (ATN). Thalamic input differentially affects presubicular neurons: layer 3 pyramidal neurons and fast-spiking parvalbumin expressing (PV) interneurons are directly and monosynaptically activated, with depressing dynamics, while somatostatin (SST) expressing interneurons are indirectly excited, during repetitive ATN activity. This arrangement ensures that the thalamic excitation of layer 3 cells is often followed by disynaptic inhibition. Feed-forward inhibition is largely mediated by PV interneurons which have a high probability of connection to presubicular pyramidal cells. Our data point to a specific role of presubicular microcircuits in shaping thalamic head-direction signals transmitted to medial entorhinal cortex: Short-latency PV cell activation may enforce temporally precise head direction tuning during fast turns. However, depression at ATN-PV synapses during repeated activation tends to facilitate pyramidal cell firing when head direction is maintained. Operations performed in presubicular layer 3 circuits seem welladapted for spatial fine-tuning of head direction signals sent to the medial entorhinal cortex.All rights reserved. No reuse allowed without permission.

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Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum

Cited by 47 publications

References 83 publications

Recurrent connections between CA2 pyramidal cells

Recurrent connections between CA2 pyramidal cells

Multiple two-photon targeted whole-cell patch-clamp recordings from monosynaptically connected neurons in vivo

Anterior thalamic excitation and feed-forward inhibition of presubicular neurons projecting to medial entorhinal cortex

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