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Grid cell co-activity patterns during sleep reflect spatial overlap of grid fields during active behaviors.

ABSTRACT: Continuous-attractor network models of grid formation posit that recurrent connectivity between grid cells controls their patterns of co-activation. Grid cells from a common module exhibit stable offsets in their periodic spatial tuning curves across environments, and this may reflect recurrent connectivity or correlated sensory inputs. Here we explore whether cell-cell relationships predicted by attractor models persist during sleep states in which spatially informative sensory inputs are absent. We recorded ensembles of grid cells in superficial layers of medial entorhinal cortex during active exploratory behaviors and overnight sleep. Per grid cell pair and collectively, and across waking, rapid eye movement sleep and non-rapid eye movement sleep, we found preserved patterns of spike-time correlations that reflected the spatial tuning offsets between these grid cells during active exploration. The preservation of cell-cell relationships across waking and sleep states was not explained by theta oscillations or activity in hippocampal subregion CA1. These results indicate that recurrent connectivity within the grid cell network drives grid cell activity across behavioral states.

SUBMITTER: Trettel SG

PROVIDER: S-EPMC7412059 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Grid cell co-activity patterns during sleep reflect spatial overlap of grid fields during active behaviors.

Trettel Sean G SG Trimper John B JB Hwaun Ernie E Fiete Ila R IR Colgin Laura Lee LL

Nature neuroscience 20190325 4

Continuous-attractor network models of grid formation posit that recurrent connectivity between grid cells controls their patterns of co-activation. Grid cells from a common module exhibit stable offsets in their periodic spatial tuning curves across environments, and this may reflect recurrent connectivity or correlated sensory inputs. Here we explore whether cell-cell relationships predicted by attractor models persist during sleep states in which spatially informative sensory inputs are absen ...[more]

PMID: 30911183

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Project description:We previously suggested that abnormal sleep behaviors, i.e., as found in parasomnias, may often be the expression of increased activity of the reward system during sleep. Because nightmares and sleepwalking predominate during REM and NREM sleep respectively, we tested here whether exploratory excitability, a waking personality trait reflecting high activity within the mesolimbic dopaminergic (ML-DA) system, may be associated with specific changes in REM and NREM sleep patterns in these two sleep disorders.Twenty-four unmedicated patients with parasomnia (12 with chronic sleepwalking and 12 with idiopathic nightmares) and no psychiatric comorbidities were studied. Each patient spent one night of sleep monitored by polysomnography. The Temperament and Character Inventory (TCI) was administered to all patients and healthy controls from the Geneva population (n = 293).Sleepwalkers were more anxious than patients with idiopathic nightmares (Spielberger Trait anxiety/STAI-T), but the patient groups did not differ on any personality dimension as estimated by the TCI. Compared to controls, parasomnia patients (sleepwalkers together with patients with idiopathic nightmares) scored higher on the Novelty Seeking (NS) TCI scale and in particular on the exploratory excitability/curiosity (NS1) subscale, and lower on the Self-directedness (SD) TCI scale, suggesting a general increase in reward sensitivity and impulsivity. Furthermore, parasomnia patients tended to worry about social separation persistently, as indicated by greater anticipatory worry (HA1) and dependence on social attachment (RD3). Moreover, exploratory excitability (NS1) correlated positively with the severity of parasomnia (i.e., the frequency of self-reported occurrences of nightmares and sleepwalking), and with time spent in REM sleep in patients with nightmares.These results suggest that patients with parasomnia might share common waking personality traits associated to reward-related brain functions. They also provide further support to the notion that reward-seeking networks are active during human sleep.

Dataset Information

Grid cell co-activity patterns during sleep reflect spatial overlap of grid fields during active behaviors.

Publications

Grid cell co-activity patterns during sleep reflect spatial overlap of grid fields during active behaviors.

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