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Ion-channel regulation of response decorrelation in a heterogeneous multi-scale model of the dentate gyrus.

ABSTRACT: Heterogeneities in biological neural circuits manifest in afferent connectivity as well as in local-circuit components such as neuronal excitability, neural structure and local synaptic strengths. The expression of adult neurogenesis in the dentate gyrus (DG) amplifies local-circuit heterogeneities and guides heterogeneities in afferent connectivity. How do neurons and their networks endowed with these distinct forms of heterogeneities respond to perturbations to individual ion channels, which are known to change under several physiological and pathophysiological conditions? We sequentially traversed the ion channels-neurons-network scales and assessed the impact of eliminating individual ion channels on conductance-based neuronal and network models endowed with disparate local-circuit and afferent heterogeneities. We found that many ion channels differentially contributed to specific neuronal or network measurements, and the elimination of any given ion channel altered several functional measurements. We then quantified the impact of ion-channel elimination on response decorrelation, a well-established metric to assess the ability of neurons in a network to convey complementary information, in DG networks endowed with different forms of heterogeneities. Notably, we found that networks constructed with structurally immature neurons exhibited functional robustness, manifesting as minimal changes in response decorrelation in the face of ion-channel elimination. Importantly, the average change in output correlation was dependent on the eliminated ion channel but invariant to input correlation. Our analyses suggest that neurogenesis-driven structural heterogeneities could assist the DG network in providing functional resilience to molecular perturbations.

SUBMITTER: Mishra P

PROVIDER: S-EPMC7610774 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The ability of a neuronal population to effectuate channel decorrelation, which is one form of response decorrelation, has been identified as an essential prelude to efficient neural encoding. To what extent are diverse forms of local and afferent heterogeneities essential in accomplishing channel decorrelation in the dentate gyrus (DG)? Here, we incrementally incorporated four distinct forms of biological heterogeneities into conductance-based network models of the DG and systematically delineate their relative contributions to channel decorrelation. First, to effectively incorporate intrinsic heterogeneities, we built physiologically validated heterogeneous populations of granule (GC) and basket cells (BC) through independent stochastic search algorithms spanning exhaustive parametric spaces. These stochastic search algorithms, which were independently constrained by experimentally determined ion channels and by neurophysiological signatures, revealed cellular-scale degeneracy in the DG. Specifically, in GC and BC populations, disparate parametric combinations yielded similar physiological signatures, with underlying parameters exhibiting significant variability and weak pair-wise correlations. Second, we introduced synaptic heterogeneities through randomization of local synaptic strengths. Third, in including adult neurogenesis, we subjected the valid model populations to randomized structural plasticity and matched neuronal excitability to electrophysiological data. We assessed networks comprising different combinations of these three local heterogeneities with identical or heterogeneous afferent inputs from the entorhinal cortex. We found that the three forms of local heterogeneities were independently and synergistically capable of mediating significant channel decorrelation when the network was driven by identical afferent inputs. However, when we incorporated afferent heterogeneities into the network to account for the divergence in DG afferent connectivity, the impact of all three forms of local heterogeneities was significantly suppressed by the dominant role of afferent heterogeneities in mediating channel decorrelation. Our results unveil a unique convergence of cellular- and network-scale degeneracy in the emergence of channel decorrelation in the DG, whereby disparate forms of local and afferent heterogeneities could synergistically drive input discriminability.

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Ion-channel regulation of response decorrelation in a heterogeneous multi-scale model of the dentate gyrus.

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