Exposure to complex environments results in more sparse representations of space in the hippocampus

Abstract

The neural circuitry mediating sensory and motor representations is adaptively tuned by an animal's interaction with its environment. Similarly, higher order representations such as spatial memories can be modified by exposure to a complex environment (CE), but in this case the changes in brain circuitry that mediate the effect are less well understood. Here we show that prolonged CE exposure was associated with increased selectivity of CA1 “place cells” to a particular recording arena compared to a social control (SC) group. Furthermore, fewer CA1 and DG neurons in the CE group expressed high levels of Arc protein, a marker of recent activation, following brief exposure to a completely novel environment. The reduced Arc expression was not attributable to overall changes in cell density or number. These data indicate that one effect of CE exposure is to modify high-level spatial representations in the brain by increasing the sparsity of population coding within networks of neurons. Greater sparsity could result in a more efficient and compact coding system that might alter behavioural performance on spatial tasks. The results from a behavioural experiment were consistent with this hypothesis, as CE-treated animals habituated more rapidly to a novel environment despite showing equivalent initial responding.

Hippocampal subfield‐specific Homer1a expression is triggered by learning‐facilitated long‐term potentiation and long‐term depression at medial perforant path synapses

“…The differentiated IEG encoding by hippocampal subfields of learning‐facilitated LTD may reflect this cumulative learning process and the involvement of LTD in the fine‐tuning and modification of an established neuronal network. In line with this pruning hypothesis, it has been shown that the acquisition of knowledge about complex spatial environments is associated with greater sparsity of neuronal activation coupled with more robust neuronal encoding (Bilkey et al, 2017). By contrast, induction of LTP increases the physical capacity and dimensions of hippocampal synapses (Bromer et al, 2018).…”

Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices

“…EE has profound effects on memory processing, including the formation, consolidation, and retrieval of spatial and declarative memory (Bilkey et al, 2017 ; Ohline and Abraham, 2019 ; Smail et al, 2020 ). The mechanisms underlying this cognitive function have been intensely studied during the past decades, including experience-dependent tuning of single neurons (e.g., place cells) and complex multi-neuronal patterns which are formed on top of coherent network oscillations (Wilson and McNaughton, 1994 ; Lee and Wilson, 2002 ; Frank et al, 2006 ; Klausberger and Somogyi, 2008 ).…”

“…At the network level, changes in the number and function of inhibitory interneurons lead to changes in excitation-inhibition ratio, favoring increased activity of cortical principal cells (Sale et al, 2007 ; Greifzu et al, 2014 ). Finally, recordings from freely behaving rats have shown selective changes in multi-cellular representations of spatial contexts including increased sparsity and increased propensity to the remapping of place cells (Bilkey et al, 2017 ). Together, exposure of rodents to enriched environments results in multiple alterations at different system levels which, together, increase behavioral flexibility and adaptation.…”

Virtual reality video game improves high-fidelity memory in older adults

“…The potential to stimulate plasticity and up-regulate function in the hippocampus has been demonstrated in rodent model studies using spatial exploration of novel, complex environs [20][21][22][23] . Specifically, spatial navigation tasks have been applied to achieve environmental enrichment in animals [24][25][26][27] , which refers to exposure and learning of novel and complex information that have been linked to the vitality of the memory system in the brain 21 . Moreover, in a study with younger adults, who played five-hours in a visually complex video game, participants improved their capability for high-fidelity LTM, relative to placebo control 28 .…”

“…The results from a growing literature show a decline in mnemonic discrimination capability for nondemented older adults 1 , as well as associated aging-related changes in functional activity in the hippocampal region 19 .The potential to stimulate plasticity and up-regulate function in the hippocampus has been demonstrated in rodent model studies using spatial exploration of novel, complex environs [20][21][22][23] . Specifically, spatial navigation tasks have been applied to achieve environmental enrichment in animals [24][25][26][27] , which refers to exposure and learning of novel and complex information that have been linked to the vitality of the memory system in the brain 21 . Moreover, in a study with younger adults, who played five-hours in a visually complex video game, participants improved their capability for high-fidelity LTM, relative to placebo control 28 .We developed a virtual reality (VR) spatial wayfinding game as a cognitive intervention aimed to mimic environmental enrichment approaches used in the study of animals with the goal of improving, and potentially restoring, memory abilities in healthy older adults.…”