A cortical cell ensemble in the posterior parietal cortex controls past experience-dependent memory updating

Suzuki, Akinobu; Kosugi, Sakurako; Murayama, Emi; Sasakawa, Eri; Ohkawa, Noriaki; Konno, Ayumu; Hirai, Hirokazu; Inokuchi, Kaoru

doi:10.1038/s41467-021-27763-x

Cited by 17 publications

(17 citation statements)

References 46 publications

(58 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The PPC serves as a cortical integration site for hippocampally generated allocentric spatial information and egocentric spatial orientation to permit goal-directed navigation ( 19 , 35 – 37 ). Further, memory reactivation during sleep has been observed in the parietal cortex as in the PFC ( 33 , 38 ), and the importance of PPC-PFC pathway for memory updating was recently highlighted ( 39 ). Therefore, the other behaviors may also elicit sleep-related consolidation effects, but these may not involve the PPC due to absence of goal-directed behavior and because the Plusmaze is the only task of the three that utilized a compartment structure.…”

Section: Discussionmentioning

confidence: 99%

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Aleman‐Zapata

Morris

Genzel

2022

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Memory reactivation during non–rapid-eye-movement ripples is thought to communicate new information to a systems-wide network and thus can be a key player mediating the positive effect of sleep on memory consolidation. Causal experiments disrupting ripples have only been performed in multiday training paradigms, which decrease but do not eliminate memory performance, and no comparison with sleep deprivation has been made. To enable such investigations, we developed a one-session learning paradigm in a Plusmaze and show that disruption of either sleep with gentle handling or hippocampal ripples with electrical stimulation impaired long-term memory. Furthermore, we detected hippocampal ripples and parietal high-frequency oscillations after different behaviors, and a bimodal frequency distribution in the cortical events was observed. Faster cortical high-frequency oscillations increased after normal learning, a change not seen in the hippocampal ripple-disruption condition, consistent with these having a role in memory consolidation.

show abstract

Section: Discussionmentioning

confidence: 99%

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Aleman‐Zapata

Morris

Genzel

2022

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…To investigate the effect of anesthesia on retrograde amnesia, we used sevoflurane treatment combined with a hippocampus-dependent memory task: the CPFE paradigm ( Ghandour et al, 2019 ; Ohkawa et al, 2015 ; Rudy and O'Reilly, 2001 ; Schiffino et al, 2011 ; Suzuki et al, 2022 ). In this paradigm ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To test this hypothesis, we assessed the effect of sevoflurane, a volatile general anesthetic, on memory function using a hippocampus-dependent memory task, context pre-exposure facilitation effect (CPFE) paradigm ( Fanselow, 1990 ; Ghandour et al, 2019 ; Ohkawa et al, 2015 ; Rudy and O'Reilly, 2001 ; Schiffino et al, 2011 ; Suzuki et al, 2022 ). In the CPFE paradigm mice have to learn the association of context information presented first with foot shock experience delivered later.…”

Section: Introductionmentioning

confidence: 99%

Sevoflurane-induced amnesia is associated with inhibition of hippocampal cell ensemble activity after learning

et al. 2022

Self Cite

View full text Add to dashboard Cite

General anesthesia could induce amnesia, however the mechanism remains unclear. We hypothesized that suppression of neuronal ensemble activity in the hippocampus by anesthesia during the post-learning period causes retrograde amnesia. To test this hypothesis, two experiments were conducted with sevoflurane anesthesia (2.5%, 30 min): a hippocampus-dependent memory task, the context pre-exposure facilitation effect (CPFE) procedure to measure memory function and in vivo calcium imaging to observe neural activity in hippocampal CA1 during context exploration and sevoflurane/home cage session. Sevoflurane treatment just after context pre-exposure session impaired the CPFE memory, suggesting sevoflurane induced retrograde amnesia. Calcium imaging showed sevoflurane treatment prevented neuronal activity in CA1. Further analysis of neuronal activity with non-negative matrix factorization, which extracts neural ensemble activity based on synchronous activity, showed that sevoflurane treatment reduced the reactivation of neuronal ensembles between during context exploration just before and one day after sevoflurane inhalation. These results suggest that sevoflurane treatment immediately after learning induces amnesia, resulting from suppression of reactivation of neuronal ensembles.

show abstract

“…Silencing the PPC specifically during the inter-trial interval affected the behavioral performance of rats (Akrami et al, 2018; Hwang et al, 2017), whereas silencing during the stimulus presentation did not affected performance. The PPC is also reciprocally connected to hippocampus via entorhinal and retrosplenial cortices (Save and Poucet, 2009; Whitlock et al, 2008) and to basolateral amygdala via the anterior cingulate cortex (Suzuki et al, 2022), giving fast access to the different memory hubs. Khodagholy et al(Khodagholy et al, 2017) showed coupling of PPC and hippocampal ripples that strengthen in non-REM sleep after rats learned a spatial exploration task, further indicating that RL may relay history information from subcortical memory hubs to cortex.…”

Section: Discussionmentioning

confidence: 99%

“…But do these areas that participate in the learning process also carry history information? Encoding of history information has been reported mainly in higher order cortical areas such as the posterior parietal cortex (PPC) (Akrami et al, 2018;Harvey et al, 2012;Hwang et al, 2017;Morcos and Harvey, 2016;Suzuki et al, 2022) , retrosplenial cortex (Hattori et al, 2019;Vann et al, 2009) and prefrontal cortex (Banerjee et al, 2020;Johnson et al, 2016;Kawai et al, 2015;Sul et al, 2010;Tsutsui et al, 2016) , but also to a smaller extent in lower-order primary sensory areas such as BC (Banerjee et al, 2020;Chéreau et al, 2020;Rodgers et al, 2021). There is still a debate on which areas link history information with the learning process.…”

Section: Introductionmentioning

confidence: 99%

History information emerges in the cortex during learning

Marmor

Helmchen

Gilad

2022

Preprint

View full text Add to dashboard Cite

We learn from our experience but the underlying neuronal mechanisms incorporating past information to facilitate learning is relatively unknown. Specifically, which cortical areas encode history-related information and how is this information modulated across learning? To study the relationship between history and learning, we continuously imaged cortex-wide calcium dynamics as mice learn to use their whiskers to discriminate between two different textures. We mainly focused on comparing the same trial type with different history information, i.e., a different preceding trial. We found history information in barrel cortex (BC) during stimulus presentation. Importantly, history information in BC emerged only as the mouse learned the task. Next, we also found learning-dependent history information in rostrolateral (RL) association cortex that emerges before stimulus presentation, preceding activity in BC. History information was also found in other cortical areas and was not related to differences in body movements. Interestingly, a binary classifier could discriminate history information at the single trial level just as well as current information both in BC and RL. These findings suggest that past experience emerges in the cortex around the time of learning, starting from higher-order association area RL and propagating down (i.e., top-down projection) to lower-order BC where it can be integrated with incoming sensory information. This integration between the past and present may facilitate learning.

show abstract

A cortical cell ensemble in the posterior parietal cortex controls past experience-dependent memory updating

Cited by 17 publications

References 46 publications

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Sevoflurane-induced amnesia is associated with inhibition of hippocampal cell ensemble activity after learning

History information emerges in the cortex during learning

Contact Info

Product

Resources

About