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Network-centered homeostasis through inhibition maintains hippocampal spatial map and cortical circuit function.

ABSTRACT: Despite ongoing experiential change, neural activity maintains remarkable stability. Although this is thought to be mediated by homeostatic plasticity, what aspect of neural activity is conserved and how the flexibility necessary for learning and memory is maintained is not fully understood. Experimental studies suggest that there exists network-centered, in addition to the well-studied neuron-centered, control. Here we computationally study such a potential mechanism: input-dependent inhibitory plasticity (IDIP). In a hippocampal model, we show that IDIP can explain the emergence of active and silent place cells as well as remapping following silencing of active place cells. Furthermore, we show that IDIP can also stabilize recurrent dynamics while preserving firing rate heterogeneity and stimulus representation, as well as persistent activity after memory encoding. Hence, the establishment of global network balance with IDIP has diverse functional implications and may be able to explain experimental phenomena across different brain areas.

SUBMITTER: Kaleb K

PROVIDER: S-EPMC8411119 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Despite half-a-century of research since the seminal work of Hubel and Wiesel, the role of the dorsal lateral geniculate nucleus (dLGN) in shaping the visual signals is not properly understood. Placed on route from retina to primary visual cortex in the early visual pathway, a striking feature of the dLGN circuit is that both the relay cells (RCs) and interneurons (INs) not only receive feedforward input from retinal ganglion cells, but also a prominent feedback from cells in layer 6 of visual cortex. This feedback has been proposed to affect synchronicity and other temporal properties of the RC firing. It has also been seen to affect spatial properties such as the center-surround antagonism of thalamic receptive fields, i.e., the suppression of the response to very large stimuli compared to smaller, more optimal stimuli. Here we explore the spatial effects of cortical feedback on the RC response by means of a a comprehensive network model with biophysically detailed, single-compartment and multicompartment neuron models of RCs, INs and a population of orientation-selective layer 6 simple cells, consisting of pyramidal cells (PY). We have considered two different arrangements of synaptic feedback from the ON and OFF zones in the visual cortex to the dLGN: phase-reversed ('push-pull') and phase-matched ('push-push'), as well as different spatial extents of the corticothalamic projection pattern. Our simulation results support that a phase-reversed arrangement provides a more effective way for cortical feedback to provide the increased center-surround antagonism seen in experiments both for flashing spots and, even more prominently, for patch gratings. This implies that ON-center RCs receive direct excitation from OFF-dominated cortical cells and indirect inhibitory feedback from ON-dominated cortical cells. The increased center-surround antagonism in the model is accompanied by spatial focusing, i.e., the maximum RC response occurs for smaller stimuli when feedback is present.

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Network-centered homeostasis through inhibition maintains hippocampal spatial map and cortical circuit function.

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