Anatomical Organization and Spatiotemporal Firing Patterns of Layer 3 Neurons in the Rat Medial Entorhinal Cortex

Tang, Qiusong; Ebbesen, Christian Laut; Sanguinetti-Scheck, Juan Ignacio; Preston-Ferrer, Patricia; Gundlfinger, Anja; Winterer, Jochen; Beed, Prateep; Ray, Saikat; Naumann, Robert K.; Schmitz, Dietmar; Brecht, Michael; Burgalossi, Andrea

doi:10.1523/jneurosci.0696-15.2015

Cited by 50 publications

(60 citation statements)

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“…Previous descriptions of modular distribution of histochemical markers in superficial layers of MEC of rodents include clusters of calbindin-positive cells (Fujimaru and Kosaka, 1996), zinc-positive terminals (Slomianka and Geneser, 1997) and acetylcholinesterase patches (Slomianka and Geneser, 1991), yet the interrelation of these different markers was unknown. Here we show that, in addition to the recently described calbindin-patches which overlap with AChE activity (Ray et al, 2014), the MEC contains a complementary modular system, involving dendrites of PCP4-positive L3 and L5 pyramidal cells overlapping with zinc activity ( Figure 6 ; Tang et al, 2015). Interestingly, presynaptic zinc and PCP4 seem to have overlapping or complementary distribution throughout the entire hippocampal region (Ishihara and Fukuda, 2016).…”

Section: Discussionsupporting

confidence: 60%

“…The apical dendrites of PCP4-positive cells from layers 3 and 5 of MEC bundle in MEC layer 2 (Tang et al, 2015). Thus, we tested whether PCP4-positive apical dendrites co-localize with the zinc modules.…”

Section: Resultsmentioning

confidence: 99%

“…Calretinin cells form translaminar clusters with the highest density of cells in layer 3 (Miettinen et al, 1997). Pyramidal cells in layers 3 and 5 are displayed as in Figure 3 of Witter and Moser (2006); they form dendritic bundles, which terminate in between calbindin patches (Hamam et al, 2000; van Haeften et al, 2003; Wouterlood et al, 2004; Witter and Moser, 2006; Tang et al, 2015). …”

Section: Discussionmentioning

confidence: 99%

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Complementary Modular Microcircuits of the Rat Medial Entorhinal Cortex

Ray

Burgalossi

Brecht

et al. 2017

Front. Syst. Neurosci.

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The parahippocampal region is organized into different areas, with the medial entorhinal cortex (MEC), presubiculum and parasubiculum prominent in spatial memory. Here, we also describe a region at the extremity of the MEC and bordering the subicular complex, the medial-most part of the entorhinal cortex. While the subdivisions of hippocampus proper form more or less continuous cell sheets, the superficial layers of the parahippocampal region have a distinct modular architecture. We investigate the spatial distribution, laminar position, and putative connectivity of zinc-positive modules in layer 2 of the MEC of rats and relate them to the calbindin-positive patches previously described in the entorhinal cortex. We found that the zinc-positive modules are complementary to the previously described calbindin-positive patches. We also found that inputs from the presubiculum are directed toward the zinc-positive modules while the calbindin-positive patches received inputs from the parasubiculum. Notably, the dendrites of neurons from layers 3 and 5, positive for Purkinje Cell Protein 4 expression, overlap with the zinc modules. Our data thus indicate that these two complementary modular systems, the calbindin patches and zinc modules, are part of parallel information streams in the hippocampal formation.

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Section: Discussionsupporting

confidence: 60%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Complementary Modular Microcircuits of the Rat Medial Entorhinal Cortex

Ray

Burgalossi

Brecht

et al. 2017

Front. Syst. Neurosci.

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“…Many previous studies have identified a substantial subset of mEC cells as nonspatial (Kropff et al, ; Latuske et al, ; Tang et al, ; Tang et al, ; Zhang et al, ). In contrast, recent work utilizing more sophisticated classification criteria found that almost all mEC cells exhibit some degree of spatial firing (Diehl et al, ; Hardcastle, Maheswaranathan, et al, ).…”

Section: Discussionmentioning

confidence: 99%

Stability of medial entorhinal cortex representations over time

Diehl¹,

Hon²,

Leutgeb³

et al. 2018

Hippocampus

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Distinct functional cell types in the medial entorhinal cortex (mEC) have been shown to represent different aspects of experiences. To further characterize mEC cell populations, we examined whether spatial representations of neurons in mEC superficial layers depended on the scale of the environment and changed over extended time periods. Accordingly, mEC cells were recorded while rats repeatedly foraged in a small or a large environment in sessions that were separated by time intervals from minutes to hours. Comparing between large and small environments, we found that the overall precision of grid and non-grid cell spatial maps was higher in smaller environments. When examining the stability of spatial firing patterns over time, differences and similarities were observed across cell types. Within-session stability was higher for grid cells than for non-grid cell populations. Despite differences in baseline stability between cell types, stability levels remained consistent over time between sessions, up to 1 hr. Even for sessions separated by 6 hrs, activity patterns of grid cells and of most non-grid cells lacked any systematic decrease in spatial similarity over time. However, a subset of ~15% of mEC non-grid cells recorded preferentially from layer III exhibited dramatic, time dependent changes in firing patterns across 6 hrs, reminiscent of previous characterizations of the hippocampal CA2 subregion. Collectively, our data suggest that mEC grid cell input to hippocampus in conjunction with many time invariant non-grid cells may aid in stabilizing hippocampal spatial maps, while a subset of time varying non-grid cells could provide complementary temporal information.

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“…Specifically, two layer 2 subtypes were classified as RELN + and one as CALB1 + (Witter et al, 2017). Other upper-layer subtypes were depicted based on marker gene expression of LAMA3 , PDGFD , IL1RAPL2 , and PCP4 (Ramsden et al, 2015; Tang et al, 2015; Ohara et al, 2018). The middle-to-deep layer subtypes were delineated by the specific gene expression of RORB , THEMIS , ADRA1A , and TLE4 .…”

Section: Methodsmentioning

confidence: 99%

Molecular Diversity Among Adult Human Hippocampal and Entorhinal Cells

Franjic

Choi

Škarica

et al. 2020

Preprint

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RESULTS 104Transcriptomic diversity of hippocampal and entorhinal cells 105 To survey the transcriptomic diversity and functional specification of the mesial temporal 106 cortex, we used snRNA-seq to profile five subregions of the hippocampal-entorhinal system 107 6 collected from fresh frozen postmortem brains of clinically unremarkable human donors. These 108 specimens were selected from a larger pool of postmortem human brains based on the quality 109 of isolated nuclei and RNA. Taking into consideration dramatic cytoarchitectonic variations, 110 we microdissected the hippocampal formation (DG, CA2-4, CA1, and subiculum) and EC for 111 a total of five subregions (Fig. 1A). 112 Unbiased isolation of nuclei using our previously described protocol (Li et al., 2018; 113 Zhu et al., 2018) followed by snRNA barcoding, cDNA sequencing and quality filtering yielded 114 108,315 high-quality single-nucleus profiles from all five subregions ( Fig. 1A, S1A-D). 115 Analysis of the expression of genes known to be enriched in major cell subpopulations 116 suggested these included 44,697 neurons, of which 35,768 (80.02%) were glutamatergic 117 excitatory neurons (expressing the gene encoding the vesicular glutamate transporter SLC17A7) 118 and 8,929 (19.98%) were GABAergic inhibitory neurons (expressing the gene encoding the 119 GABA synthesis enzyme GAD1), reflecting the expected 80:20 ratio of these populations. In 120 addition, we identified 63,618 (58.73% of the total population) non-neuronal cells. 121 We next analyzed the transcriptomes of those nuclei on the Uniform Manifold 122 Approximation and Projection (UMAP) layout representing their similarities at cellular 123 granularity ( Fig. 1B-D). Iterative clustering defined 69 transcriptomically distinct cell clusters 124 representing presumptive cell types across all individuals (donors). These transcriptomically 125 diverse subpopulations were organized into a dendrogramatic taxonomy reflecting their gene 126 expression patterns and were subsequently assigned identities commensurate with predicted cell 127 types. This allowed us to identify 26 subtypes of excitatory neurons (Fig. 1E and S2A-B), 23 128 inhibitory neuron subtypes ( Fig. 1E and S2C-D), and 20 non-neuronal cell types and subtypes 129 ( Fig. 1E and S2E-F). Similar single nucleus approaches applied to human neocortical samples 130 7 yielded comparable numbers and distributions of cell populations in medial temporal gyrus 131 (MTG) (Hodge et al., 2019)and dorso-lateral prefrontal cortex (dlPFC) (Li et al., 2018)(Fig. 132 S1E-F). 133Within excitatory neuron subtypes, we found marked transcriptional diversity that 134 reflects differences in the cytoarchitectonic organization among the subregions of the HIP (DG, 135 CA2-4, CA1, and subiculum) and EC (Fig. 1E). For example, in addition to ADCYAP1-136 expressing mossy cells in DG, we found three distinct subclusters of PROX1-expressing granule 137 cells. We also identified excitatory neurons in CA1 and CA2-4 that could be deconstructe...

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Anatomical Organization and Spatiotemporal Firing Patterns of Layer 3 Neurons in the Rat Medial Entorhinal Cortex

Cited by 50 publications

References 50 publications

Complementary Modular Microcircuits of the Rat Medial Entorhinal Cortex

Complementary Modular Microcircuits of the Rat Medial Entorhinal Cortex

Stability of medial entorhinal cortex representations over time

Molecular Diversity Among Adult Human Hippocampal and Entorhinal Cells

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