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

ArticleinNature Neuroscience 13(2):213-22 · February 2010with11 Reads
DOI: 10.1038/nn.2458 · Source: PubMed
Abstract
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.
    • "DDi projects to Vd and Vc, components of the striatum () and we have previously argued (Sas et al., 1993) that this region can also be considered as ventral striatum. There is also a functional parallel in that both hilar (Williams et al., 2007; Larimer and Strowbridge, 2010) and DDmg/DDi (Elliott and Maler, 2015) neurons exhibit Up states. "
    [Show abstract] [Hide abstract] ABSTRACT: Teleost fish are capable of complex behaviours including social and spatial learning; lesion studies show that these abilities require dorsal telencephalon (pallium). The teleost telencephalon has subpallial and pallial components. The subpallium is well described and highly conserved. In contrast, the teleost pallium is not well understood and its relation to that of other vertebrates remains controversial. Here we analyze the connectivity of the subdivisions of dorsal pallium (DD) of an electric gymnotiform fish, Apteronotus leptorhynchus: superficial (DDs), intermediate (DDi) and magnocellular (DDmg) components. The major pathways are recursive: the dorsolateral pallium (DL) projects strongly to DDi with lesser inputs to DDs and DDmg. DDi in turn projects strongly to DDmg which then feeds back diffusely to DL. Our quantitative analysis of DDi connectivity demonstrates that it is a global recurrent network. In addition, we show that the DD subnuclei have complex reciprocal connections with subpallial regions. Specifically, both DDi and DDmg are reciprocally connected to pallial interneurons within the misnamed rostral entopeduncular nucleus (Er). Based on DD connectivity, we illustrate the close similarity, and possible homology, between hippocampal and DD/DL circuitry. We hypothesize that DD/DL circuitry can implement the same pattern separation and completion computations ascribed to the hippocampal dentate gyrus and CA3 fields. We further contend that the DL to DDi to DDmg to DL feedback loop makes the pattern separation/completion operations recursive. We discuss our results with respect to recent studies on fear avoidance conditioning in zebrafish and attention and spatial learning in a pulse gymnotiform fish. This article is protected by copyright. All rights reserved.
    Full-text · Article · Jun 2016
    • "This is the first report identifying the shared electrophysiological similarity of these neuron types. Intriguingly, each of these neuron types exhibits low-threshold and persistent spiking activity at theta-band frequencies (Gentet et al. 2012; Hayar et al. 2004; Larimer and Strowbridge 2010; Pressler and Strowbridge 2006) and thus may share the computational function of driving or triggering recurrent network theta rhythms. Similarly, we observed a large cluster of high R input , broad spiking cells from the midbrain and brainstem, including the ventral tegmental area and locus coeruleus. "
    [Show abstract] [Hide abstract] ABSTRACT: For decades, neurophysiologists have characterized the biophysical properties of a rich diversity of neuron types. However, identifying common features and computational roles shared across neuron types is made more difficult by inconsistent conventions for collecting and reporting biophysical data. Here, we leverage NeuroElectro, a literature-based database of electrophysiological properties (www.neuroelectro.org), to better understand neuronal diversity -- both within and across neuron types -- and the confounding influences of methodological variability. We show that experimental conditions (e.g., electrode types, recording temperatures, or animal age) can explain a substantial degree of the literature-reported biophysical variability observed within a neuron type. Critically, accounting for experimental metadata enables massive cross-study data normalization and reveals that electrophysiological data are far more reproducible across labs than previously appreciated. Using this normalized dataset, we find that neuron types throughout the brain cluster by biophysical properties into 6-9 super-classes. These classes include intuitive clusters, such as fast-spiking basket cells, as well as previously unrecognized clusters, including a novel class of cortical and olfactory bulb interneurons that exhibit persistent activity at theta-band frequencies. Copyright © 2015, Journal of Neurophysiology.
    Full-text · Article · Mar 2015
    • "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). "
    [Show abstract] [Hide abstract] 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.
    Full-text · Article · Mar 2015
    Bo WangBo WangLuping YinLuping YinXiaolong ZouXiaolong Zou+1more author...[...]
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