What role can a representation of space that
is divorced from the present moment play in a
navigating animal? Egyptian fruit bats navi-
gate landscapes spanning hundreds of kilometers
to forage for food, flying in highly reproducible
paths to and from foraging sites ( 1 ). Members
of this species also make novel shortcuts be-
tween distant foraging sites ( 3 , 4 ). This suggests
that during goal-directed navigation, these bats
maintain a detailed spatial memory of both
their environment and of paths taken within
it. To understand how this nonlocal code may
be used for path-based, goal-directed naviga-
tion, we engaged animals in a freely paced
foraging task in an automated environment
[Fig. 2A; ( 31 ); see the supplementary materials
and methods]. Four reward feeders positioned
along one wall of the room fed at different
probabilities, with one side feeding at higher
probabilities than the other (e.g., 70 and 30%).
The probabilities switched after a set number
of feeds to induce exploration to all feeders and
to keep the animals attentive to the task (see
the supplementary materials and methods).
We recorded neural activity from three bats
engaged in the goal-directed foraging task. One
bat performed the task alone and the other two
performed the task at the same time (204 of 281
total cells were sufficiently active during be-
havior; see the supplementary materials and
methods). There were no differences in the
results between the individual bat and the
pair, nor were there any indications of social
representations of the other bat under the
conditions of this experiment (fig. S10). We
therefore combined the data from all three bats
in subsequent analyses. Bats formed common
paths, and typically only visited the feeders and
a few places in the room to rest between feed-
ings (Fig. 2B). Individual bats developed distinct
movement patterns (fig. S11), underscoring
the self-selected nature and reproducibility of
their flight paths during goal-directed naviga-
tion (fig. S11B).To determine whether nonlocal positions
are encoded during foraging, we performed
the same time-shifting analysis as in the ran-
dom exploration experiments, focusing on the
flights occurring along reproducible paths. Be-
cause flight paths were constrained to narrow
portions of the room, leading to a heteroge-
neous sampling of thezaxis with respect to
thexandyaxes, we constrained the analysis
to 2D, as was done previously [(32, 33); similar
results were found in 3D; fig. S12]. Similar to
the random exploration experiment (Fig. 1),
neural activity predominantly encoded non-
local positions, was again shifted toward the
future, and maintained a consistent level of
spatial information for all temporal lags (Fig.
2, C and D, and fig. S12). Results were robust to
multiple shuffle tests designed to account for
the flight pattern structure (fig. S13; see the
supplementary materials and methods). We
found a very high percentage of neurons with
significant spatial information (90%, 183/204244 9JULY2021•VOL 373 ISSUE 6551 sciencemag.org SCIENCE
Fig. 2. Nonlocal spatiotemporal coding is present during goal-directed
navigation.(A) Illustration of the foraging task (not drawn to scale; room
dimensions: 5.6 m × 5.2 m × 2.5 m). Bats choose between four different feeders.
Feeders fed at predetermined probabilities that switched during the session
(see the supplementary materials and methods). (B) Left: all the flights on
repeatable paths (black lines) are shown for a single recording session. Non-path
flights are shown in gray. Right: break out of individual flight paths. Each
subplot represents a distinct flight path (see the supplementary materials and
methods). (C) Rate maps for three examples neurons with maximum spatial
information at future time shifts. Top: all flight data. Middle: parts of flights with
heading angles toward the feeders. Bottom: parts of flights with heading
angles toward the stands. Maximum firing rate and bias-corrected spatial information
values are as follows: left, max fr. = 30.98 Hz, lag zero = 0.65 bits, optimal
lag = 1.08 bits; middle, max fr. = 56.11 Hz, lag zero = 0.49 bits, optimal lag =
0.93 bits; and right, max fr. = 9.76 Hz, lag zero = 0 bits (n.s.), optimal lag =
0.37 bits. (D) Cumulative sum of peak spatial information (top) and bias-corrected
spatial information across lags. The 25th (bottom gray line), 50th (middle
black line), and 75th (top gray line) percentiles are shown. (E) Top-down view
showing the locations of spatiotemporal field centers. Color code indicates
time lag of maximal spatial information.RESEARCH | REPORTS