Selection of preconfigured cell assemblies for representation of novel spatial experiences

Abstract

Internal representations about the external world can be driven by the external stimuli or can be internally generated in their absence. It has been a matter of debate whether novel stimuli from the external world are instructive over the brain network to create de novo representations or, alternatively, are selecting from existing pre-representations hosted in preconfigured brain networks. The hippocampus is a brain area necessary for normal internally generated spatial-temporal representations and its dysfunctions have resulted in anterograde amnesia, impaired imagining of new experiences, and hallucinations. The compressed temporal sequence of place cell activity in the rodent hippocampus serves as an animal model of internal representation of the external space. Based on our recent results on the phenomenon of novel place cell sequence preplay, we submit that the place cell sequence of a novel spatial experience is determined, in part, by a selection of a set of cellular firing sequences from a repertoire of existing temporal firing sequences in the hippocampal network. Conceptually, this indicates that novel stimuli from the external world select from their pre-representations rather than create de novo our internal representations of the world.

Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation

“…Certain cells can be predicted to express place fields prior to exposure to a novel environment based on their participation in pre-play (Dragoi and Tonegawa, 2011, 2013, 2014), suggesting experience-dependent synaptic plasticity plays little to no role in the appearance of these fields since their inputs are already able to drive firing prior to the experience. Place fields that engage pre-strengthened inputs could appear immediately upon exposure to novel environments, or even following a delayed period, as changes in attention could later activate these pathways (Monaco et al, 2014).…”

“…Additionally, many place fields are immediately present upon the animal’s first traversal across a novel environment (Frank et al, 2004; Hill, 1978). Such a rapidly appearing cognitive map suggests that hippocampal representations could arise through the novel stimulus dependent selection of pre-strengthened neuronal ensembles (Deguchi et al, 2011; Dragoi and Tonegawa, 2011, 2013, 2014; Lee et al, 2012). These results call into question the idea that place fields form de novo through synaptic plasticity during experience of a novel environment.…”

Time cells in the hippocampus: a new dimension for mapping memories

“…Although it is easy to imagine the compression of firing chains by simply having fewer spikes per cell and the subsequent decompression as longer spike bursts, a reproduction of an externally generated representation of real-time context representations would require a more complex compression mechanism that allows decompression to reconstruct the original intervals. Furthermore, hippocampal neuronal firing sequences that can be observed prior to learning subsequently characterize the sequences of place-cell firing in maze performance 70 . Conversely, firing sequences persisted in a mouse model of neurodegeneration associated with a loss of spatial sequence coding, which is consistent with the existence of temporal firing chains prior to representations of events 71 .…”

CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus

“…The simplest scenario would be a random allocation of place cells 116 to maximize the separation of neuronal representations in different environments (‘pattern separation’ or remapping 117–119 ). However, recent experiments challenge this model, demonstrating that firing rate distributions of CA1PCs are skewed (log-normally distributed) 120 , the firing activity of each cell is largely preserved across behavioral states 120 , and hippocampal PCs may even be, at least in part, preselected for activation 121,122 . Other results also indicate that high-firing-rate, diffusely firing neurons may form a stable ‘backbone’, over which plastic low-firing-rate cells ‘learn’ to encode for highly specific aspects of the environment 123 .…”