Functional properties of stellate cells in medial entorhinal cortex layer II

Rowland, David C; Obenhaus, Horst A.; Skytøen, Emilie R; Zhang, Qiangwei; Kentros, Clifford; Moser, Edvard I; Moser, May‐Britt

doi:10.7554/elife.36664

Cited by 84 publications

(80 citation statements)

References 71 publications

(118 reference statements)

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“…Grid cells provide input to the hippocampus (7 ) and are assumed to be the primary determinant of hippocampal place cell firing (3,5,8). However, this notion has been challenged by the fact that place cells appear before grid cells during development (9,10).…”

Section: Introductionmentioning

confidence: 99%

Perineuronal nets stabilize the grid cell network

Christensen

Lensjø

Lepperød

et al. 2019

Preprint

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Grid cells are part of a widespread network that supports navigation and spatial memory. Stable grid patterns appear late in development, in concert with extracellular matrix aggregates termed perineuronal nets (PNNs) that condense around inhibitory neurons. To reveal the relationship between stable spatial representations and the presence of PNNs we recorded from populations of neurons in adult rats. We show that removal of PNNs leads to lower inhibitory spiking activity, and reduces grid cells' ability to create stable representations of a novel environment. Furthermore, in animals with disrupted PNNs, exposure to a novel arena corrupted the spatiotemporal relationships within grid cell modules, and the stored representations of a familiar arena. Finally, we show that PNN removal in entorhinal cortex distorted spatial representations in downstream hippocampal neurons. Together this work suggests that PNNs provide a key stabilizing element for the grid cell network.(9, 11). Once established, the periodic spiking pattern of grid cells is remarkably stable when animals revisit the same environment. Local perturbations of different cell types in MEC cause changes to grid field spike rates or an increased number of out-of-field spikes, but the location of the fields remains unaltered (12)(13)(14). Furthermore, when placed in a different environment, neighboring populations of grid cells show a coherent shift of grid fields (15) that retains their relative spatiotemporal relationships (16). In contrast the hippocampal place cells remap by independently and unpredictably changing their activity. This suggests that the mature grid cell network is more hardwired and less plastic than the hippocampal place cell network.The network that controls grid cell spiking is not yet fully understood, but recurrent inhibition appears to be fundamental to the specific activity of grid cells. Stellate cells, one of the two principal cell types that display grid cell firing (7 ), are connected via parvalbumin expressing (PV + ) inhibitory interneurons (17 , 18). PV + cells account for about 50% of the inhibitory cells in MEC (19), making them the main inhibitory mediator in the local grid cell network. In sensory cortex, PV + cells play a central role in shaping the excitatory activity of principal neurons by regulating the onset of periods of high synaptic plasticity (20). Whether PV + inhibitory neurons in MEC play a similar role for development of the grid cell network remains elusive.A hallmark of maturing PV + cells is that aggregates of specialized extracellular matrix, called perineuronal nets (PNNs), condense on the cell soma and proximal dendrites, leaving openings only for synaptic connections (21). PNNs are believed to help stabilize the activity of PV + cells by supporting synaptic integrity and limiting synaptogenesis, in addition to supporting PV + cell physiology (22). By the time PNNs in sensory cortex are fully mature, plasticity in the local network is strongly reduced. However, juvenile levels of plasticity can be r...

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Section: Introductionmentioning

confidence: 99%

Perineuronal nets stabilize the grid cell network

Christensen

Lensjø

Lepperød

et al. 2019

Preprint

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“…Stellate cells are the most populous cell type comprising nearly 70 % of principal neurons in layer II of the MEC. Of these, one in four are grid cells 3,25,26 .The receptive fields of different grid cells form an overlapping patchwork that covers space 3 (Figure 3a). Within a localized region of the MEC, grid cell receptive fields share the same spatial frequency and orientation, but are phase-shifted with respect to each other.…”

Section: Resultsmentioning

confidence: 99%

Theta oscillations gate the transmission of reliable sequences in the medial entorhinal cortex

Neru

Assisi

2019

Preprint

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Reliable sequential activity of neurons in the entorhinal cortex is necessary to encode spatially guided behavior and memory. In a realistic computational model of a medial entorhinal cortex (MEC) microcircuit, with stellate cells coupled via a network of inhibitory interneurons, we show how intrinsic and network mechanisms interact with theta oscillations to generate reliable outputs. Sensory inputs activate interneurons near their most excitable phase during each theta cycle. As the inputs change, different groups of interneurons are recruited and postsynaptic stellate cells are released from inhibition causing a sequence of rebound spikes. Since the rebound time scale of stellate cells matches theta oscillations, its spikes get relegated to the least excitable phase of theta ensuring that the network encodes only the external drive and ignores recurrent excitation by rebound spikes. In the absence of theta, rebound spikes compete with external inputs and disrupt the sequence that follows.Our simulations concur with experimental data that show, subduing theta oscillations disrupts the spatial periodicity of grid cell receptive fields. Further, the same mechanism where theta modulates the gain of incoming inputs may be used to select between competing sources of input and create transient functionally connected networks. * collins@iiserpune.ac.in

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“…In the crab stomatogastric ganglion, inter-animal variation correlates with circuit performance (Goaillard et al, 2009) . Accordingly, variation in intrinsic properties of SCs might correlate with differences in grid firing (Domnisoru et al, 2013;Gu et al, 2018;Rowland et al, 2018;Schmidt-Hieber and Häusser, 2013) or behaviours that rely on SCs (Kitamura et al, 2014;Qin et al, 2018;Tennant et al, 2018) . It is interesting in this respect that there appear to be inter-animal differences in the spatial scale of grid modules (cf.…”

Section: Functional Consequences Of Within Cell Type Inter-animal Varmentioning

confidence: 99%

Inter- and intra-animal variation of integrative properties of stellate cells in the medial entorhinal cortex

Pastoll

Garden

Papastathopoulos

et al. 2019

Preprint

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Distinctions between cell types underpin organisational principles for nervous system function. Functional variation also exists between neurons of the same type. This is exemplified by correspondence between grid cell spatial scales and synaptic integrative properties of stellate cells (SCs) in the medial entorhinal cortex. However, we know little about how functional variability is structured either within or between individuals. Using ex-vivo patch-clamp recordings from up to 55 SCs per mouse, we find that integrative properties vary between mice and, in contrast to modularity of grid cell spatial scales, have a continuous dorsoventral organisation. Our results constrain mechanisms for modular grid firing and provide evidence for inter-animal phenotypic variability among neurons of the same type. We suggest that neuron type properties are tuned to circuit level set points that vary within and between animals.

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Functional properties of stellate cells in medial entorhinal cortex layer II

Cited by 84 publications

References 71 publications

Perineuronal nets stabilize the grid cell network

Perineuronal nets stabilize the grid cell network

Theta oscillations gate the transmission of reliable sequences in the medial entorhinal cortex

Inter- and intra-animal variation of integrative properties of stellate cells in the medial entorhinal cortex

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