Dentate gyrus granule cell firing patterns can induce mossy fiber long‐term potentiation in vitro

Mistry, Rajen B.; Dennis, Siobhan; Frerking, Matthew; Mellor, Jack R.

doi:10.1002/hipo.20815

Cited by 30 publications

(38 citation statements)

References 39 publications

(62 reference statements)

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“…Stimulation-induced synaptic discharges led to somatic depolarization that was sufficient for the cell to fire, and we varied the stimulus strength from trial to trial so that the rise time of somatic depolarization before the first AP ranged from 5–8 to 100–200 ms. This type of granule cell activity is well within the range documented in behaving animals30. We found that in every tested cell, the spiking threshold increased robustly when the depolarization rate was slowed down (Fig.…”

Section: Resultssupporting

confidence: 84%

Neuronal adaptation involves rapid expansion of the action potential initiation site

et al. 2014

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Action potential (AP) generation is the key to information-processing in the brain. Although APs are normally initiated in the axonal initial segment, developmental adaptation or prolonged network activity may alter the initiation site geometry thus affecting cell excitability. Here we find that hippocampal dentate granule cells adapt their spiking threshold to the kinetics of the ongoing dendrosomatic excitatory input by expanding the AP-initiation area away from the soma while also decelerating local axonal spikes. Dual-patch soma–axon recordings combined with axonal Na+ and Ca2+ imaging and biophysical modelling show that the underlying mechanism involves distance-dependent inactivation of axonal Na+ channels due to somatic depolarization propagating into the axon. Thus, the ensuing changes in the AP-initiation zone and local AP propagation could provide activity-dependent control of cell excitability and spiking on a relatively rapid timescale.

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Section: Resultssupporting

confidence: 84%

Neuronal adaptation involves rapid expansion of the action potential initiation site

et al. 2014

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“…[16]. Following a post-slicing recovery period of > 1 hr slices were transferred to an interface-type recording chamber constantly perfused with artificial cerebrospinal fluid (aCSF) at 33°C.…”

Section: Methodsmentioning

confidence: 99%

Altered synaptic plasticity in the mossy fibre pathway of transgenic mice expressing mutant amyloid precursor protein

et al. 2010

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Aβ peptides derived from the cleavage of amyloid precursor protein are widely believed to play an important role in the pathophysiology of Alzheimer's disease. A common way to study the impact of these molecules on CNS function is to compare the physiology of transgenic mice that overproduce Aβ with non-transgenic animals. In the hippocampus, this approach has been frequently applied to the investigation of synaptic transmission and plasticity in the perforant and Schaffer collateral commissural pathways, the first and third components of the classical hippocampal trisynaptic circuit, respectively. Similar studies however have not been carried out on the remaining component of the trisynaptic circuit, the mossy fibre pathway. Using transverse hippocampal slices prepared from ~2 year old animals we have compared mossy fibre synaptic function in wild-type mice and their Tg2576 littermates which age-dependently overproduce Aβ. Input-output curves were not altered in slices from Tg2576 mice, but these animals exhibited a significant loss of the prominent frequency-facilitation expressed by the mossy fibre pathway. In addition to this change in short term synaptic plasticity, high frequency stimulation-induced, NMDA-receptor-independent LTP was absent in slices from the transgenic mice. These data represent the first description of functional deficits in the mossy fibre pathway of Aβ-overproducing transgenic mice.

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“…It is perhaps surprising that so few granule cells discharge during normal behavior (Alme et al, 2010) and at such low firing frequencies (<0.2 Hz; Jung and McNaughton, 1993). More recent studies, however, report that higher spike frequencies (averaging about 1 Hz) normally occur (Leutgeb et al, 2007; Mistry et al, 2011). Moreover, during behavioral tasks, many perforant path axons conduct impulses at rates of 10–20 Hz or more (Fyhn et al, 2007), while granule cells may generate high frequency bursts of impulses (Mistry et al, 2011).…”

Section: Implications Of the Lamellar Hypothesis For Understanding Dementioning

confidence: 98%

Updating the Lamellar Hypothesis of Hippocampal Organization

Sloviter¹,

Lømo²

2012

Front. Neural Circuits

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Andersen et al. (1971) proposed that excitatory activity in the entorhinal cortex propagates topographically to the dentate gyrus, and on through a “trisynaptic circuit” lying within transverse hippocampal “slices” or “lamellae.” In this way, a relatively simple structure might mediate complex functions in a manner analogous to the way independent piano keys can produce a nearly infinite variety of unique outputs. The lamellar hypothesis derives primary support from the “lamellar” distribution of dentate granule cell axons (the mossy fibers), which innervate dentate hilar neurons and area CA3 pyramidal cells and interneurons within the confines of a thin transverse hippocampal segment. Following the initial formulation of the lamellar hypothesis, anatomical studies revealed that unlike granule cells, hilar mossy cells, CA3 pyramidal cells, and Layer II entorhinal cells all form axonal projections that are more divergent along the longitudinal axis than the clearly “lamellar” mossy fiber pathway. The existence of pathways with “translamellar” distribution patterns has been interpreted, incorrectly in our view, as justifying outright rejection of the lamellar hypothesis (Amaral and Witter, 1989). We suggest that the functional implications of longitudinally projecting axons depend not on whether they exist, but on what they do. The observation that focal granule cell layer discharges normally inhibit, rather than excite, distant granule cells suggests that longitudinal axons in the dentate gyrus may mediate “lateral” inhibition and define lamellar function, rather than undermine it. In this review, we attempt a reconsideration of the evidence that most directly impacts the physiological concept of hippocampal lamellar organization.

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Dentate gyrus granule cell firing patterns can induce mossy fiber long‐term potentiation in vitro

Cited by 30 publications

References 39 publications

Neuronal adaptation involves rapid expansion of the action potential initiation site

Neuronal adaptation involves rapid expansion of the action potential initiation site

Altered synaptic plasticity in the mossy fibre pathway of transgenic mice expressing mutant amyloid precursor protein

Updating the Lamellar Hypothesis of Hippocampal Organization

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