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Notably, the properties of our Fos-high ensembles are similar to those of
place cells that participate in sharp-wave ripples   48
.") .
For example, similarly to Fos-high cells, place cells that are modulated by
sharp-wave ripples have fields that evenly tile the entire environment, are
not biased towards the reward location and are stable over time   48
.") ,
 49 .") . These
similarities suggest that our Fos-high ensembles may be involved in memory
consolidation during quiet wakefulness or sleep, as sharp-wave ripple events
occur during these periods and contain compressed replay or reactivation of
place cell sequences critical for stable spatial memories   50
.") .
##  A causal role for Fos in spatial coding
* 29k  Accesses
77. Yatsenko, D. et al. DataJoint: managing big scientific data using MATLAB or Python. Preprint at _bioRxiv_  https://doi.org/10.1101/031658  (2015).
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###   Extended Data Fig. 8 Place field remapping and Fos-induction across
multiple virtual environments in the absence of a task.
_Nature Communications_ (2023)
###  Cross-day alignment of sources
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Fos-high cells had larger integrated ∆ _F_ / _F_ values, and thus larger total
calcium influx, relative to Fos-low cells (Fig.  1j
 ), in line with the known role of
increased calcium influx in driving gene transcription through voltage-
sensitive calcium channels  31  ,  32  ,  33
.") . The
larger calcium influx in Fos-high cells did not arise from a substantially
greater number of calcium transients per second but rather resulted mainly
from higher integrated calcium levels per transient (Fig.  1k,l
 ). The higher calcium influx per
transient was due to longer transients rather than a change in the amplitude
of transients (Fig.  1m,n  ). Because
previous work has shown that calcium transients in pyramidal neuron cell
bodies are related to spiking  34  ,  35  , [ 36
](/articles/s41586-022-05113-1#ref-CR36 "Evans, S. W. et al. A positively
tuned voltage indicator reveals electrical correlates of calcium activity in
the brain. Preprint at bioRxiv
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Jordan S. Farrell, Ernie Hwaun, … Ivan Soltesz
Table 3
Statistics for Figure 3
(E–H) Same as (A)–(D) but for One-Way sequences.
###  Place field properties
https://doi.org/10.1101/061507
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Source data
We used a miniaturized modified version of a visual virtual reality system  
58 .") that has been described
previously   42 .") . Head-restrained mice ran on an air-supported spherical treadmill
that was constrained with a yaw and roll blocker to rotate only in pitch
(forwards and backwards relative to the mouse’s body). Ball movement was
detected by two optical sensors (ADNS-9800, Avago Technologies) connected to a
Teensy-3.2 microcontroller (PJRC.com) mounted to a custom printed circuit
board. Forward translation in the virtual environment was controlled by
rotation of the ball, with velocity gain adjusted such that distance travelled
in the virtual environment equalled the distance travelled on the surface of
the ball. The virtual environment was back-projected (laser pico-bit
projector, Celluon) onto a parabolic screen surrounding ~180 degrees of the
mouse in azimuth, with a minimum screen distance from the mouse of
approximately 5 inches. Designs for the virtual reality and behaviour hardware
can be found at  https://github.com/HarveyLab/mouseVR
 . Water rewards were delivered through
a spout, with a solenoid valve controlling reward timing and quantity. Licks
were detected by an electrical circuit triggered by contact with the lick
spout.
It is noteworthy that the relationship between neural activity and Fos is
bidirectional. Beyond serving as a marker of behaviourally relevant neurons,
once induced, Fos acts as a critical regulator of gene expression programmes
controlling cellular, synaptic and circuit modifications that in turn fine-
tune network activity   11 .") ,  22  ,
23  ,  24 .") . However, while both engram and cognitive map
theories indicate that synaptic plasticity occurs to stabilize hippocampal
memories   25 .") ,  26
.") , few studies have investigated the
function of Fos as an inroad to a deeper understanding of the mechanisms of
memory formation, consolidation and retrieval.
###   Extended Data Fig. 3 Enrichment of Fos expression in navigation-related
areas after virtual navigation.
####  Acute slice preparation
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###  Reporting summary
The virtual track was constructed using the Virtual Reality Mouse Engine
(ViRMEn)   59 .") in MATLAB (Mathworks).
The end of the track was continuous with its beginning, such that the track
repeated with a circular topology. The walls of the track were tiled with
textures to serve as visual landmarks. In the no-task and remapping
experiments, two additional linear-track environments were introduced that
were visually distinct with an inter-trial interval of 5 s.
In summary, there were two possible sequences:
Second, we reasoned that, if Fos-high cells are related to place codes, then
Fos induction should track the identity of place cells across different
environments   18 .") . As expected, when mice were moved to
virtual environments with distinct visual cues, the place code remapped   37
.") , including in Fos-
high place cells (Extended Data Fig.  8a–g
 ). During remapping, a cell’s Fos
induction in an environment was related to whether the cell had a place field
(Extended Data Fig.  8l,m  ). Of cells
without a place field in one environment, those that gained a place field in a
second environment were more likely to have high Fos induction in the second
environment than those that continued to lack a place field (Extended Data
Fig.  8o  , top). Additionally, of cells
with a place field in one environment, those that lost their place field in a
second environment were less likely to have high Fos induction in the second
environment than cells that had a place field in both environments (Extended
Data Fig.  8o  , bottom). Thus, Fos-high
cells remapped in a manner consistent with place cells, and Fos induction
tended to track the presence of a place field, even across multiple
environments.
Mice were transported from the housing facility in a light-blocked cart and
kept in a dim experimental room throughout the day to minimize unintended Fos
expression. Mice were trained to lick for water rewards in a hidden reward
zone one-tenth the length of the track (20 cm). Before being exposed to the
virtual environment, mice were habituated to the apparatus and trained to run
and lick the water spout to receive rewards. Once mice transitioned into the
virtual environment, the task contingency was fixed and water rewards were
delivered after the first lick in the reward zone. Occasionally, manual
rewards were delivered to ensure that the lick detection and reward delivery
systems were working; trials with manual rewards were excluded from further
analysis. In the final version of the behavioural task, mice were required to
traverse the linear track and lick in a specific reward zone to receive water
rewards   48 .") ,  60 .") ,  61 .") . Three trial types were
present within each session: standard, crutch and probe. In standard trials
(60–70% of trials), a water reward was delivered after the first lick in the
reward zone. In crutch trials (20–30% of trials), a water reward was delivered
as soon as the mouse entered the reward zone, regardless of licking behaviour.
In probe trials (less than 10% of trials), no rewards were delivered,
regardless of the mouse’s licking behaviour. Probe trials allowed us to assess
licking and running behaviour in the absence of rewards. For standard and
crutch trials, licks that occurred in the reward zone after the delivery of
reward were deemed ‘consumption licks’ and did not contribute to measures of
licking selectivity or numbers of licks. All other licks were considered ‘test
licks’ (non-consumption licks). Muscimol inactivation experiments were
performed in an earlier version of the task where the size of the reward zone
was 40 cm rather than 20 cm.
###  Behaviour analysis
Towards this goal, we recently demonstrated that Fos orchestrates cell-type-
specific inhibitory plasticity in the hippocampal CA1 region and that Fos
function is required for hippocampus-dependent spatial learning in the Morris
water maze   24 .") . These results suggest that Fos might
modulate place codes, given the known influence of inhibition on place cell
firing and the likely role of place cells in spatial learning   16
.") ,  27 .") ,  28 .") . However, it remained to
be determined whether Fos in fact has an active role in regulating aspects of
place cell function during spatial navigation.
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* ###   A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions
##  Robust place coding in Fos-high neurons
After alignment across days, individual cells in mice with conditional Fos
knockout were manually examined for Cre–GFP expression. Cre probability maps
were produced from aligned Cre–GFP images using Cellpose   75
.") . Cells were manually examined taking
into account their source mask as well as jRGECO1a, Cre–GFP and Cre
probability images. Cells were manually labelled as Cre  \+  (Fos-KO), Cre  –
(wild type) or ambiguous. Ambiguous cells were excluded from further analysis.
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###  Surgery: virus injection
66. Pachitariu, M. et al. Suite2p: beyond 10,000 neurons with standard two-photon microscopy. Preprint at _bioRxiv_  https://doi.org/10.1101/061507  (2017).
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###  Virtual environment
Everton J. Agnes & Tim P. Vogels
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We observed significant differences in the neural activity of Fos-KO cells
relative to their wild-type neighbours. Fos-KO cells had fewer calcium
transients per second (Fig.  3d  ) but
higher integrated calcium levels and longer calcium transient durations (Fig.
 3c,e,g  ), indicating that Fos has a
cell-autonomous role in altering neuronal activity levels. Other aspects of
activity in Fos-KO cells were similar to those in wild-type cells, such as the
peak amplitude of transients (Fig.  3f 
). In brain slice experiments, Fos-KO and wild-type cells had similar calcium
influx per spike along with similar calcium transient kinetics and intrinsic
electrophysiological properties, indicating that Fos is not involved in
regulating these cellular properties (Extended Data Fig.  9
 ). Thus, Fos-KO cells have altered
calcium transients during the navigation task but normal calcium influx per
spike, suggesting that Fos-KO cells have different numbers or patterns of
spikes relative to wild-type cells. Although our experiments lack the
resolution to determine what these differences in spiking are, they
nevertheless demonstrate that disruption of Fos has specific effects on a
cell’s activity in mice during navigation.
##  Activity features of Fos-high neurons
###   Source Data Extended Data Fig. 9
1. Noah L. Pettit
###  Muscimol
##  Comments
###  Histology
Many factors can contribute to variability in the mean decoding accuracy
across different positions of the track, including running speed, the
configuration of visual cues   74 .") and behavioural
variability. In particular, higher running speeds in the region of the track
away from the reward zone, combined with the relatively slow kinetics of the
calcium indicator, probably contributed to the increased decoding error there.
We therefore focused on comparing groups of neurons recorded simultaneously
and treated identically during analysis. Decoding analyses were always
performed on size-matched subpopulations, and testing and training frames were
identical for each subpopulation tested.
###   Source Data Fig. 4
(M) Example foraging rate maps.
(L–N) Same as (I)–(K) but for One-Way sequences.
Show results from  All journals  This journal
##  This article is cited by
Before ex vivo electrophysiological recordings, _Fos_ _fl_ / _fl_ ; _Fosb_
_fl_ / _fl_ ; _Junb_ _fl_ / _fl_ mice were injected with AAV-Cre-GFP to
conditionally disrupt the Fos complex in a sparse subset of CA1 neurons, as
previously described   24 .") . Surgical preparation and procedures
up to virus injection were carried out as described in the surgery methods for
in vivo experiments. Mice at 3–4 weeks of age were anaesthetized by isoflurane
inhalation and placed in a stereotaxic frame (Kopf, model 1900). A small
craniotomy was made on the dorsal surface of the skull, and virus injection
was performed bilaterally using bevelled glass micropipettes targeted to CA1
(ML: ±3.0 mm; AP: −2.4 mm; dorsal/ventral, DV: −2.8 mm). Approximately 1 μl of
AAV2/1-CAG-Cre-GFP (titre of 1.751 × 10  11  genome copies per ml) was
injected at a rate of 150 nl min  –1  , after which the pipette was left in
place for approximately 5 min to allow the virus to diffuse and pressure to
dissipate before retraction. Mice were allowed to recover for at least 7 days
to allow for virus expression and recombination to occur.
Given the decreased reliability across trials, lower spatial selectivity and
smaller fraction of cells with place fields in the Fos-KO population, we
reasoned that Fos-KO cells might form less accurate spatial maps than their
wild-type neighbours. We tested how well we could predict a mouse’s spatial
location from the activity of equally sized populations of Fos-KO and wild-
type cells. The accuracy of decoding the mouse’s location was lower when using
the activity in the Fos-KO population than when using that in the wild-type
population (Fig.  3m  ).
###   Source Data Extended Data Fig. 5
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Together, these results point towards a causal role for Fos in shaping
hippocampal function during spatial navigation. However, we note that Fos is
not required for the expression of place fields, given that many Fos-KO cells
had place fields. This finding might be expected because place fields arise
within minutes in an environment   40 .") , which is faster than Fos
induction and its downstream effects   11 .")
,  23 .") . Instead, Fos has a causal role in regulating the activity
properties of CA1 neurons and contributes to the expression of place codes
with high reliability and accuracy.
\(2021\).") , these findings may reflect different spiking patterns in Fos-high and Fos-low cells   10 .") . However, the relationship between spiking and calcium transients may also be different for these groups of cells. To test the latter possibility, we compared the spike-evoked calcium influx in cells with and without Fos induction using current-clamp recordings and calcium imaging in brain slices (Extended Data Fig.  5a–c  ). Cells with Fos induction had smaller calcium transients in response to triggered action potentials, a finding that warrants future investigation. The kinetics of calcium transients and intrinsic electrophysiological properties were similar to those in cells without Fos induction (Extended Data Fig.  5d–k  ). Therefore, Fos-high cells have higher total calcium influx during the navigation task and Fos-expressing cells have lower calcium influx per spike ex vivo, suggesting that Fos-induced cells may have more spiking or a different pattern of spiking than non-Fos-induced cells. Although we could not resolve the precise underlying in vivo spiking patterns associated with Fos induction, our results indicate that prolonged elevated calcium may have an important role in inducing the expression of Fos during a navigation task.
(B) Number of place fields in each session.