Maturation of long‐term potentiation in the hippocampal dentate gyrus of the freely moving rat

Bronzino, Joseph D.; Abu-Hasaballah, Khamis; Austin-LaFrance, R.J.; Morgane, Peter J.

doi:10.1002/hipo.450040406

Cited by 47 publications

(18 citation statements)

References 20 publications

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“…To test retention of the task, the platform was removed for a 60-s probe test 4 hr after the last trial on day 6. Mice that had been trained with four trials per day spent more time in the platform quadrant than in all others (controls, F (3,28) ϭ 57.17, P Ͻ 0.0001; runners, F (3,28) ϭ 16.70, P Ͻ 0.0001). Mice trained with two trials per day did not show a significant preference for the platform quadrant (controls, F (3,32) ϭ 1.53, P Ͼ 0.23; runners, F (3,32) ϭ 2.56, P Ͻ 0.07), although for runners, the trend appeared stronger (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Although newborn cells are a small percentage of the total cells in the granule cell layer, it is possible that new neurons affect hippocampal physiology more than do mature cells (27). Indeed, in immature rats, dentate gyrus LTP lasts longer than in adults (28). Newborn cells in the adult brain may be similar to those generated during development.…”

Section: Discussionmentioning

confidence: 99%

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Running enhances neurogenesis, learning, and long-term potentiation in mice

Praag

Christie

Sejnowski

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

2,532

106

1,804

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Running increases neurogenesis in the dentate gyrus of the hippocampus, a brain structure that is important for memory function. Consequently, spatial learning and long-term potentiation (LTP) were tested in groups of mice housed either with a running wheel (runners) or under standard conditions (controls). Mice were injected with bromodeoxyuridine to label dividing cells and trained in the Morris water maze. LTP was studied in the dentate gyrus and area CA1 in hippocampal slices from these mice. Running improved water maze performance, increased bromodeoxyuridine-positive cell numbers, and selectively enhanced dentate gyrus LTP. Our results indicate that physical activity can regulate hippocampal neurogenesis, synaptic plasticity, and learning. N ew neurons are added continuously to certain areas of the adult brain, such as the hippocampus and olfactory bulb (1, 2). The functional significance of new hippocampal cells is not clear. In birds, food storage and retrieval experience correlate with changes in hippocampal size and neurogenesis (3). In mice, neurogenesis in the dentate gyrus increases with exposure to an enriched environment, and it is associated with improved learning (4). Similarly, voluntary physical activity in a running wheel enhances the number of new hippocampal cells (5). Although it is not known whether running also affects learning, it has been shown that physical activity facilitates recovery from injury (6) and improves cognitive function (7). Furthermore, trophic factors, associated with progenitor cell survival and differentiation (8), alterations in synaptic strength (9), long-term potentiation (LTP) (10), and memory function (11), are elevated after exercise (12, 13). At the cellular level, wheel running enhances the firing rate of hippocampal cells in a manner that correlates with running velocity (14). Thus, exercise may increase synaptic plasticity and learning, as well as neurogenesis. We designed the following experiments to test this hypothesis. Materials and MethodsSubjects. Thirty-four female C57BL͞6 mice, 3 months old (The Jackson Laboratory) were divided into two groups of 17, the controls and the runners. The runners had free access to a running wheel equipped with an electronic counter. During the first 10 days animals received one 10-mg͞ml intraperitoneal injection of 5-bromodeoxyuridine (BrdU; Sigma), dissolved in 0.9% NaCl, filtered sterile at 0.2 m, at 50 g͞g of body weight per day to label dividing cells.Spatial Learning. The mice were trained on a Morris water maze (15) with either two or four trials per day for 6 days. The platform was hidden 1 cm below the surface of water; it was made opaque with white nontoxic paint. The starting points were changed every day. Each trial lasted either until the mouse had found the platform or for a maximum of 40 s. At the end of each trial, the mice were allowed to rest on the platform for 10 s. The time to reach the platform (latency), the length of swim path, and the swim speed were recorded semi-automatically by a video trackin...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Running enhances neurogenesis, learning, and long-term potentiation in mice

Praag

Christie

Sejnowski

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

2,532

106

1,804

View full text Add to dashboard Cite

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“…The slope of the fEPSP is an indicator of the synaptic strength (Bronzino et al, 1994). We did not observe significant changes in the inputoutput relationship between the stimulus intensity and fEPSP slopes in wild-types (n 5 8) relative to mutants (n 5 7; Fig.…”

Section: Basal Synaptic Transmission At Perforant Path-granule Cell (mentioning

confidence: 89%

Reduced excitability in the dentate gyrus network of βIV‐spectrin mutant mice in vivo

et al. 2009

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The submembrane cytoskeletal meshwork of the axon contains the scaffolding protein betaIV-spectrin. It provides mechanical support for the axon and anchors membrane proteins. Quivering (qv(3j)) mice lack functional betaIV-spectrin and have reduced voltage-gated sodium channel (VGSC) immunoreactivity at the axon initial segment and nodes of Ranvier. Because VGSCs are critically involved in action potential generation and conduction, we hypothesized that qv(3j) mice should also show functional deficits at the network level. To test this hypothesis, we investigated granule cell function in the dentate gyrus of anesthetized qv(3j) mice after electrical stimulation of the perforant path in vivo. This revealed an impaired input-output relationship between stimulus intensity and granule cell population spikes and an enhanced paired-pulse inhibition of population spikes, indicating a reduced ability of granule cells to generate action potentials and decreased network excitability. In contrast, the input-output curve for evoked field excitatory postsynaptic potentials (fEPSPs) and paired-pulse facilitation of fEPSPs were unchanged, suggesting normal excitatory synaptic transmission at perforant path-granule cell synapses in qv(3j) mutants. To corroborate our findings, we analyzed the influence of VGSC density reduction on dentate network activity using an established computational model of the dentate gyrus network. This in silico approach confirmed that the loss of VGSCs is sufficient to explain the electrophysiological changes observed in qv(3j) mice. Taken together, our findings demonstrate that betaIV-spectrin is required for normal granule cell firing and for physiological levels of network excitability in the mouse dentate gyrus in vivo.

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“…Although the new cells are a small percentage of the granule cell layer, several studies have indicated that they have greater plasticity than do mature cells. Indeed, in immature rats, DG LTP lasts longer than in adults (Bronzino et al 1994 ) . In another study, it was found that putative young cells had a lower threshold for LTP and were unaffected by GABA inhibition, indicating enhanced plasticity in the young cells (Wang et al 2000 ) .…”

Section: Synaptic Plasticitymentioning

confidence: 99%

Exercise and the Brain: Neurogenesis, Synaptic Plasticity, Spine Density, and Angiogenesis

Wang

Praag

2012

Functional Neuroimaging in Exercise and Sport Sciences

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This chapter focuses on the mechanisms underlying the effects of exercise on brain structural and synaptic plasticity as well as cognitive function in rodents. In normal young and aged mice wheel running increases neurotrophin, neurotransmitter, and angiogenesis levels, and enhances fi ne neuronal morphology such as dendritic branching and spine density. Speci fi c to the dentate gyrus of the hippocampus is the increase in the production of new neurons with running, which may mediate at least in part the observed improvements in learning and memory. The role of exercise in mouse models of neurodegeneration such as Alzheimer's, Parkinson's disease and Huntington's disease is also evaluated and found to be generally bene fi cial with the potential exception of Huntington's disease. Furthermore, possible peripheral triggers elicited with exercise, such as muscle activation, that lead to improvements in brain structure and function are discussed.

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Maturation of long‐term potentiation in the hippocampal dentate gyrus of the freely moving rat

Cited by 47 publications

References 20 publications

Running enhances neurogenesis, learning, and long-term potentiation in mice

Running enhances neurogenesis, learning, and long-term potentiation in mice

Reduced excitability in the dentate gyrus network of βIV‐spectrin mutant mice in vivo

Exercise and the Brain: Neurogenesis, Synaptic Plasticity, Spine Density, and Angiogenesis

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