Local feedback inhibition tightly controls rapid formation of hippocampal place fields

Rolotti, Sebi V.; Ahmed, Mohsin; Szoboszlay, Miklos; Geiller, Tristan; Negrean, Adrian; Blockus, Heike; Gonzalez, Kevin; Sparks, Fraser T.; Canales, Ana Sofia Solis; Tuttman, Anna L; Peterka, Darcy S.; Zemelman, Boris V.; Polleux, Franck; Losonczy, Attila

doi:10.1016/j.neuron.2021.12.003

Cited by 58 publications

(61 citation statements)

References 79 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, using disinhibition, this effect can be nullified and the neural assemblies can be made larger. Rolotti et al (2022) showed such disinhibition can improve performance on a head-fixed spatial goal-oriented learning task via overrepresentation of the rewarded locations used for performance in the task. Another functional benefit of such disinhibition may be in rapid place field formation, as is seen in the behavioral timescale synaptic plasticity mechanism ( Bittner et al, 2017 ; Zhao et al, 2020 ; Milstein et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…Recent experimental evidence in mice ( Rolotti et al, 2022 ) shows that when optogenetic techniques are used to induce place field formation in CA1 neurons, feedback inhibition limits the number of neurons which become activated, thereby limiting the size of the neural assembly which becomes activated by the induced place field. However, using disinhibition, this effect can be nullified and the neural assemblies can be made larger.…”

Section: Discussionmentioning

confidence: 99%

“…In Rolotti et al (2022) , the feedback inhibition comes from the hippocampus, but they do not explore distinctions between different inhibitory populations therein. There are many different types of inhibitory neurons, each with distinct connectivity, dynamics, and morphology ( Pelkey et al, 2017 ; Burns and Rajan, 2021 ; Campagnola et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

“…We treat neurons as having a single point of intracellular space, i.e., without dendrites or specific morphology, which other than itself being unrealistic also prevents us from allowing different classes of inhibitory neurons to preferentially synapse onto different regions of other neurons, which is known to vary widely across inhibitory neurons ( Otsuka and Kawaguchi, 2009 ; Burns and Rajan, 2021 ; Dudok et al, 2021 ). We also assume that joint excitatory-inhibitory assemblies are completely connected, which is a simplification that does not match biology ( Otsuka and Kawaguchi, 2009 ; Koolschijn et al, 2019 ; Rolotti et al, 2022 ). Therefore, these and other limitations mean that whether and how actual biological networks achieve the same functional benefits we described here using inhibitory neuron diversity currently remains unknown.…”

Section: Discussionmentioning

confidence: 99%

See 3 more Smart Citations

Multiscale and Extended Retrieval of Associative Memory Structures in a Cortical Model of Local-Global Inhibition Balance

Burns

Haga

Fukai

2022

eNeuro

View full text Add to dashboard Cite

Inhibitory neurons take on many forms and functions. How this diversity contributes to memory function is not completely known. Previous formal studies indicate inhibition differentiated by local and global connectivity in associative memory networks functions to rescale the level of retrieval of excitatory assemblies. However, such studies lack biological details such as a distinction between types of neurons (excitatory and inhibitory), unrealistic connection schemas, and nonsparse assemblies. In this study, we present a rate-based cortical model where neurons are distinguished (as excitatory, local inhibitory, or global inhibitory), connected more realistically, and where memory items correspond to sparse excitatory assemblies. We use this model to study how local-global inhibition balance can alter memory retrieval in associative memory structures, including naturalistic and artificial structures. Experimental studies have reported inhibitory neurons and their subtypes uniquely respond to specific stimuli and can form sophisticated, joint excitatory-inhibitory assemblies. Our model suggests such joint assemblies, as well as a distribution and rebalancing of overall inhibition between two inhibitory subpopulations, one connected to excitatory assemblies locally and the other connected globally, can quadruple the range of retrieval across related memories. We identify a possible functional role for local-global inhibitory balance to, in the context of choice or preference of relationships, permit and maintain a broader range of memory items when local inhibition is dominant and conversely consolidate and strengthen a smaller range of memory items when global inhibition is dominant. This model, while still theoretical, therefore highlights a potentially biologically-plausible and behaviorally-useful function of inhibitory diversity in memory.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Multiscale and Extended Retrieval of Associative Memory Structures in a Cortical Model of Local-Global Inhibition Balance

Burns

Haga

Fukai

2022

eNeuro

View full text Add to dashboard Cite

show abstract

“…In all optical physiology, in some cases, it can be physiologically relevant to photostimulate a high number of cells, in particular when aiming to replicate spontaneous patterns on a mesoscale level [although there are clear evidences that the number of neurons necessary to elicit a perception is in the order of a dozen in the visual cortex ( Dalgleish et al, 2020 ), of 20 in the olfactory bulb ( Gill et al, 2020 ), on top of observations indicating the existence of possibly supralinear inhibitory mechanisms limiting the activated/activable area ( Rolotti et al, 2022 )]. This can be achieved by using lasers with higher peak powers (and lower repetition rate to maintain the average power within biologically safe limits).…”

Section: Spatio-temporal Resolution Constraints and Developments Of A...mentioning

confidence: 99%

Advantages, Pitfalls, and Developments of All Optical Interrogation Strategies of Microcircuits in vivo

Papaioannou

Medini

2022

Front. Neurosci.

View full text Add to dashboard Cite

The holy grail for every neurophysiologist is to conclude a causal relationship between an elementary behaviour and the function of a specific brain area or circuit. Our effort to map elementary behaviours to specific brain loci and to further manipulate neural activity while observing the alterations in behaviour is in essence the goal for neuroscientists. Recent advancements in the area of experimental brain imaging in the form of longer wavelength near infrared (NIR) pulsed lasers with the development of highly efficient optogenetic actuators and reporters of neural activity, has endowed us with unprecedented resolution in spatiotemporal precision both in imaging neural activity as well as manipulating it with multiphoton microscopy. This readily available toolbox has introduced a so called all-optical physiology and interrogation of circuits and has opened new horizons when it comes to precisely, fast and non-invasively map and manipulate anatomically, molecularly or functionally identified mesoscopic brain circuits. The purpose of this review is to describe the advantages and possible pitfalls of all-optical approaches in system neuroscience, where by all-optical we mean use of multiphoton microscopy to image the functional response of neuron(s) in the network so to attain flexible choice of the cells to be also optogenetically photostimulated by holography, in absence of electrophysiology. Spatio-temporal constraints will be compared toward the classical reference of electrophysiology methods. When appropriate, in relation to current limitations of current optical approaches, we will make reference to latest works aimed to overcome these limitations, in order to highlight the most recent developments. We will also provide examples of types of experiments uniquely approachable all-optically. Finally, although mechanically non-invasive, all-optical electrophysiology exhibits potential off-target effects which can ambiguate and complicate the interpretation of the results. In summary, this review is an effort to exemplify how an all-optical experiment can be designed, conducted and interpreted from the point of view of the integrative neurophysiologist.

show abstract

Optogenetic and chemogenetic studies of spatial navigation

Jarzebowski,

Hay,

Paulsen

2025

Encyclopedia of the Human Brain

View full text Add to dashboard Cite

Local feedback inhibition tightly controls rapid formation of hippocampal place fields

Cited by 58 publications

References 79 publications

Multiscale and Extended Retrieval of Associative Memory Structures in a Cortical Model of Local-Global Inhibition Balance

Multiscale and Extended Retrieval of Associative Memory Structures in a Cortical Model of Local-Global Inhibition Balance

Advantages, Pitfalls, and Developments of All Optical Interrogation Strategies of Microcircuits in vivo

Optogenetic and chemogenetic studies of spatial navigation

Contact Info

Product

Resources

About