Unique Processing During a Period of High Excitation/Inhibition Balance in Adult-Born Neurons

By A. Marin-Burgin, L. Mongiat, M. B. Pardi, A. F. Schinder. 2012

376 citations recorded by the source corpus.

Neurogenesis and Pattern Integration The adult hippocampus continuously produces new neurons that integrate into the dentate gyrus network and contribute to information processing. What features of adult-born neurons are important for information processing in the dentate gyrus? Marín-Burgin et al. (p. 1238, published online 26 January; see the Perspective by Kempermann) labeled newborn neurons and used sophisticated electrophysiological and imaging techniques to show that immature neurons integrated a broader variety of synaptic inputs from different origins compared with mature neurons, which were highly input specific. Thus, immature neurons may represent a population of integrators that are broadly tuned during a transient period and may encode most features of incoming information. After maturation, new granule cells display a high activation threshold and input specificity to become good pattern separators. A specific set of functional properties can be attributed to immature granule cells developing in the hippocampus. The adult dentate gyrus generates new granule cells (GCs) that develop over several weeks and integrate into the preexisting network. Although adult hippocampal neurogenesis has been implicated in learning and memory, the specific role of new GCs remains unclear. We examined whether immature adult-born neurons contribute to information encoding. By combining calcium imaging and electrophysiology in acute slices, we found that weak afferent activity recruits few mature GCs while activating a substantial proportion of the immature neurons. These different activation thresholds are dictated by an enhanced excitation/inhibition balance transiently expressed in immature GCs. Immature GCs exhibit low input specificity that switches with time toward a highly specific responsiveness. Therefore, activity patterns entering the dentate gyrus can undergo differential decoding by a heterogeneous population of GCs originated at different times.

Subfields: Cellular and Molecular Neuroscience, Developmental Neuroscience, Neurology

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Citations in the corpus

Re-evaluating circuit mechanisms underlying pattern separation (2019, positive): “, 2016) receive reduced synaptic inhibition (Li et al., 2012; Marin-Burgin et al., 2012; Dieni et al., 2013).”
Distinct Determinants of Sparse Activation during Granule Cell Maturation (2013, background): “These results confirm the enhanced excitability of 4-week-old GCs in response to ML stimulation (Marín-Burgin et al., 2012) and reveal that the time window for enhanced responsiveness is brief since it was not evident at 6 weeks PTI.”
Adult Neurogenesis in the Hippocampus: From Stem Cells to Behavior. (2016, positive): “As newborn neurons mature further, they come under stronger inhibitory control, and the range of stimuli that elicit firing becomes narrower, resulting in sparser activity typical of mature DGCs (Danielson et al., 2016; Marı́n-Burgin et al., 2012).”
Retrograde monosynaptic tracing reveals the temporal evolution of inputs onto new neurons in the adult dentate gyrus and olfactory bulb (2013, background): “Such ratio of inhibitory versus excitatory inputs at this stage of their functional incorporation, may reflect a developmental condition of maintaining the highly excitable new neurons (4) under strong inhibition, and could thereby contribute to the selection of the forming excitatory synapses.”
The role of adult hippocampal neurogenesis in brain health and disease (2018, background): “DGCs are responsive to a broader range of inputs [40], hyperexcitable to stimulation [41, 42], and have a lower”
Hippocampal Memory Traces Are Differentially Modulated by Experience, Time, and Adult Neurogenesis (2014, background): “Interestingly, levels of activity during encoding (number of EYFP+ cells; for recent DG versus CA3: p < 0.001; for remote DG versus CA3: p < 0.001) are higher in the DG than in CA3, which may reflect a preferential role of the DG in encoding (Kheirbek et al., 2013; Lee and Kesner, 2004).”
Hilar Mossy Cell Degeneration Causes Transient Dentate Granule Cell Hyperexcitability and Impaired Pattern Separation (2012, positive): “Whereas the activation of mature granule cells is limited by such inhibition, the impact on immature granule cells, whose activation threshold and input specificity are low (Marı́n-Burgin et al., 2012), may alter behavior.”
Maturation and integration of adult born hippocampal neurons: signal convergence onto small Rho GTPases (2013, background): “Positive extrinsic regulators include physical exercise, environmental enrichment, antidepressants, and learning, whereas stress and aging negatively regulate the number of newly generated neurons (Ma et al., 2009).”