Representing information in cell assemblies: Persistent activity mediated by semilunar granule cells

Department of Neurosciences, Case Western Reserve University, Cleveland, Ohio, USA.
Nature Neuroscience (Impact Factor: 16.1). 02/2010; 13(2):213-22. DOI: 10.1038/nn.2458
Source: PubMed


Here we found that perforant path stimulation in rat hippocampal slices evoked long-lasting barrages of synaptic inputs in subpopulations of dentate gyrus mossy cells and hilar interneurons. Synaptic barrages triggered persistent firing in hilar neurons (hilar up-states). We found that synaptic barrages originate from semilunar granule cells (SGCs), glutamatergic neurons in the inner molecular layer that generate long-duration plateau potentials in response to excitatory synaptic input. MK801, nimodipine and nickel all abolished both stimulus-evoked plateau potentials in SGCs and synaptic barrages in downstream hilar neurons without blocking fast synaptic transmission. Hilar up-states triggered functional inhibition in granule cells that persisted for more than 10 s. Hilar cell assemblies, identified by simultaneous triple and paired intracellular recordings, were linked by persistent firing in SGCs. Population responses recorded in hilar neurons accurately encoded stimulus identity. Stimulus-evoked up-states in the dentate gyrus represent a potential cellular basis for hippocampal working memory.

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    • "However , the intrinsic properties of neurons are not always ''ideal.'' For example, semilunar granule cells in the dentate gyrus can fire APs for a long duration in response to brief stimulation of the perforant pathway (Larimer and Strowbridge, 2010), and neocortical pyramidal cells (PCs) can generate graded persistent activity while metabotropic receptors are activated (Egorov et al., 2002; Sidiropoulou et al., 2009). Despite the lack of substantial evidence for the behavioral relevance of ''unideal'' neurons , theoretical studies have suggested important roles of these neurons in cortical functions (Lisman et al., 1998; Loewenstein and Sompolinsky, 2003). "
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    ABSTRACT: A critical step in understanding the neural basis of human cognitive functions is to identify neuronal types in the neocortex. In this study, we performed whole-cell recording from human cortical slices and found a distinct subpopulation of neurons with intrinsic persistent activity that could be triggered by single action potentials (APs) but terminated by bursts of APs. This persistent activity was associated with a depolarizing plateau potential induced by the activation of a persistent Na(+) current. Single-cell RT-PCR revealed that these neurons were inhibitory interneurons. This type of neuron was found in different cortical regions, including temporal, frontal, occipital, and parietal cortices in human and also in frontal and temporal lobes of nonhuman primate but not in rat cortical tissues, suggesting that it could be unique to primates. The characteristic persistent activity in these inhibitory interneurons may contribute to the regulation of pyramidal cell activity and participate in cortical processing. Copyright © 2015 The Authors. Published by Elsevier Inc. All rights reserved.
    Cell Reports 03/2015; 9(9). DOI:10.1016/j.celrep.2015.02.018 · 8.36 Impact Factor
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    • "A number of in vitro studies have attempted to ask whether in vitro networks can encode information about time or previous stimuli in a state-dependent fashion [92–94]. One group has examined this question in rodent hippocampal slices wherein different stimuli were presented to hippocampal slices via stimulation of electrodes in the perforant pathway [93,95]. Responses to stimuli were recorded during intracellular recordings of up to three simultaneously recorded hilar neurons. "
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    ABSTRACT: The discrimination and production of temporal patterns on the scale of hundreds of milliseconds are critical to sensory and motor processing. Indeed, most complex behaviours, such as speech comprehension and production, would be impossible in the absence of sophisticated timing mechanisms. Despite the importance of timing to human learning and cognition, little is known about the underlying mechanisms, in particular whether timing relies on specialized dedicated circuits and mechanisms or on general and intrinsic properties of neurons and neural circuits. Here, we review experimental data describing timing and interval-selective neurons in vivo and in vitro. We also review theoretical models of timing, focusing primarily on the state-dependent network model, which proposes that timing in the subsecond range relies on the inherent time-dependent properties of neurons and the active neural dynamics within recurrent circuits. Within this framework, time is naturally encoded in populations of neurons whose pattern of activity is dynamically changing in time. Together, we argue that current experimental and theoretical studies provide sufficient evidence to conclude that at least some forms of temporal processing reflect intrinsic computations based on local neural network dynamics.
    Philosophical Transactions of The Royal Society B Biological Sciences 03/2014; 369(1637):20120460. DOI:10.1098/rstb.2012.0460 · 7.06 Impact Factor
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    • "We recently noted a heterogeneous distribution of calbindin in the granule cells of three sympatric African murine rodent species (Cavegn et al., 2013) that in two of the species appears similar to that in the sengi, i.e., calbindin+ cells in superficial and deep cells of the gcl separated by a tier of very light or unstained cells. A morphological and functional heterogeneity defining a population at the superficial limit of the rat gcl has also been described (Williams et al., 2007; Larimer and Strowbridge, 2010). Notably, a preferential expression of calbindin in superficial granule cells is also seen in FMR1 knockout mice (Real et al., 2011), a gene encoding FMRP (fragile mental retardation protein). "
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    ABSTRACT: The brains of sengis (elephant shrews, order Macroscelidae) have long been known to contain a hippocampus that in terms of allometric progression indices is larger than that of most primates and equal in size to that of humans. In this report, we provide descriptions of hippocampal cytoarchitecture in the eastern rock sengi (Elephantulus myurus), of the distributions of hippocampal calretinin, calbindin, parvalbumin, and somatostatin, of principal neuron numbers, and of cell numbers related to proliferation and neuronal differentiation in adult hippocampal neurogenesis. Sengi hippocampal cytoarchitecture is an amalgamation of characters that are found in CA1 of, e.g., guinea pig and rabbits and in CA3 and dentate gyrus of primates. Correspondence analysis of total cell numbers and quantitative relations between principal cell populations relate this sengi to macaque monkeys and domestic pigs, and distinguish the sengi from distinct patterns of relations found in humans, dogs, and murine rodents. Calretinin and calbindin are present in some cell populations that also express these proteins in other species, e.g., interneurons at the stratum oriens/alveus border or temporal hilar mossy cells, but neurons expressing these markers are often scarce or absent in other layers. The distributions of parvalbumin and somatostatin resemble those in other species. Normalized numbers of PCNA+ proliferating cells and doublecortin-positive (DCX+) differentiating cells of neuronal lineage fall within the overall ranges of murid rodents, but differed from three murid species captured in the same habitat in that fewer DCX+ cells relative to PCNA+ were observed. The large and well-differentiated sengi hippocampus is not accompanied by correspondingly sized cortical and subcortical limbic areas that are the main hippocampal sources of afferents and targets of efferents. This points to intrinsic hippocampal information processing as the selective advantage of the large sengi hippocampus.
    Frontiers in Neuroanatomy 10/2013; 7:34. DOI:10.3389/fnana.2013.00034 · 3.54 Impact Factor
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