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R ES E A RC H

NEUROSCIENCE cillations (7 to 11 Hz) (21–24). We next examined


this temporal coding in the other’s spatial repre-
sentations. To control for confounds of the mo-
Spatial representations of self and tion of the observer, we focused on units whose
rate peaks were located in the self’s starting po-

other in the hippocampus sitions in the opposite-side rule and analyzed


the relationship between the other’s positions
and the theta phases of the spikes (n = 78 units).
Teruko Danjo,1 Taro Toyoizumi,2 Shigeyoshi Fujisawa1* Although the self was not running during the
time course of this analysis, the local field po-
An animal’s awareness of its location in space depends on the activity of place cells in tential was dominated by theta oscillations (fig.
the hippocampus. How the brain encodes the spatial position of others has not yet been S8 and SM). In contrast to the lack of theta-
identified. We investigated neuronal representations of other animals’ locations in the phase precession relative to the self’s location,
dorsal CA1 region of the hippocampus with an observational T-maze task in which one 75% of the units displayed significant theta-
rat was required to observe another rat’s trajectory to successfully retrieve a reward. phase precession as a function of the other’s
Information reflecting the spatial location of both the self and the other was jointly and location (P < 0.01) (Fig. 1, J to M). The observed
discretely encoded by CA1 pyramidal cells in the observer rat. A subset of CA1 pyramidal theta-phase precession to the other’s location
cells exhibited spatial receptive fields that were identical for the self and the other. These was consistent with that to the self’s location,
findings demonstrate that hippocampal spatial representations include dimensions for as reported previously (21–24), demonstrating
both self and nonself. that the other’s spatial information was also

S
temporally encoded in the hippocampal pyram-

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patial navigation requires the hippocampus side rules, respectively) (fig. S2) [see the supple- idal cells.
(1, 2). The cognitive map theory states that mentary materials (SM)]. We next sought to dissociate two types of
spatial recognition in the hippocampus is We first examined how the location of the units—those preferentially modulated by the
allocentric (3–5). Place cells in the hippo- other rat was represented in the opposite-side other’s position (“other-preferred cells”) and
campus are the physiological correlate of rule observational task. Firing-rate maps of the those preferentially modulated by the self’s goal
this representation because they are highly sensi- self’s positions (“self’s rate map”) and the other’s [“goal-preferred cells,” also previously described
tive to changes in landmarks and contexts (6–13). positions (“other’s rate map,” which were obtained as “prospective cells” (25, 26)]. We took advan-
The characterization of additional types of navi- by replacing the self’s positional data with the tage of the two versions of our observational
gational representations, including head-direction other’s) revealed that in addition to the expected T-maze task (Fig. 2A). Other-preferred cells fire
cells and grid cells, has promoted our understand- coding of the observer’s own position in space, when the other is located on the same side of
ing of the neural mechanisms of allocentric spatial the majority of units also displayed obvious place the side arms (left or right), irrespective of the
representations in the hippocampal-entorhinal fields for the other (Fig. 1, C to F, top). To under- rule during a given trial and, as a result, these
cortex network (14–19). The studies of these neural stand the positional relationship of the rat pair at neurons fire when the self’s goal is on a different
maps have focused on the animal’s own position the time of firing, we constructed joint rate maps side across the two conditions (Fig. 2B). This should
in space. It still remains unclear whether and by linearizing the rats’ trajectories and entering further support the allocentric representation
how spatial information of nonself, such as the them into two-dimensional x-y axes (fig. S3). of the other’s place. In contrast, goal-preferred
position of conspecifics, landmarks, and moving Here, the self’s and other’s place fields composed cells increase their firing rate only according to
objects, is represented in the hippocampus. from identical spikes were combined into a sin- the future choice of the observer. By statistically
We designed an observational T-maze task gle joint place field (Fig. 1, C to F, bottom, and comparing the other’s rate maps between the
using a pair of rats (hereafter termed “self” and fig. S4). We then examined whether these joint two versions, we defined other-preferred cells and
“other”) and investigated how the other’s position place fields were truly modulated by the other’s goal-preferred cells based on these criteria (see
is represented in the self’s hippocampus. The self positions and not a mere consequence of the the SM). We identified 58 other-preferred cells
was required to make a left/right choice to re- constraints in the positional relationships of (Fig. 2, C to G, and fig. S9) and 252 goal-preferred
trieve a reward based on the location of the other. the two rats. The null hypothesis was that the cells (Fig. 2, H and I). Although the number of
We used two versions of the task, an “opposite- firing only depended on the self’s position and other-preferred cells was smaller than that of
side rule” version in which the self rat had to was independent of the other’s. By computing goal-preferred cells, it represented 13% of the
choose the side opposite to the other’s location the surrogate firing rates that followed this null place-responsive units examined in this analysis
(Fig. 1A, fig. S1, and movie S1) and a “same-side hypothesis (see the SM) (20), we identified areas (Fig. 2F and SM), and the firing-rate peaks of both
rule” in which the self rat had to choose the same with significantly higher firing rates for the unit groups distributed all along the side arms in
side as the other rat (fig. S1 and movie S2). During other (P < 0.05) (Fig. 1, C to F, third from top, and the other’s rate maps, constituting a full spatial
the T-maze task, neuronal activity in the self’s fig. S5). A significant firing dependency on the map based on the position of the other rat (Fig. 2,
hippocampus (dorsal CA1) was recorded extra- other’s positions was detected for 85% of units G and I). Furthermore, the analysis of comparing
cellularly (n = 3 pairs of rats; 88 ± 8.1% and 84 ± (Fig. 1, G to I), indicating that the other’s spatial the correct and the error trials in the opposite-
11% correct performance with opposite-side and information was generally encoded by the place side rule resulted in similar percentages of other-
same-side rules, respectively). All analyses were cells in this T-maze task. Importantly, the sig- preferred and goal-preferred cells (fig. S10).
performed on single units with pyramidal cell nificant areas were not dependent on the self’s We next looked for another type of spatial
features and place fields in the task area (n = specific behavior or the other’s positions (Fig. 1, representation, “a common place field” for the
1298 and 1205 units with opposite-side and same- C to I). Moreover, the firing activities of most self and other, for which a unit fires when either
units were not dependent on the time periods the other or the self is in a specific spatial loca-
in the trial (fig. S6). Similar results were also tion. We found 45 units that had common place
observed when we analyzed the same-side rule fields in both the other’s and the self’s rate maps
1
Laboratory for Systems Neurophysiology, RIKEN Brain version of the task (fig. S7). under the opposite-side rule (Fig. 3, A to E, and
Science Institute, 2-1 Hirosawa, Wako, Saitama, 351-0198, In the hippocampus, spatial information is en- SM). We further tested the trajectory specificity
Japan. 2Laboratory for Neural Computation and Adaptation,
RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama,
coded not only by the average firing rates of the of common place fields by separating left- and
351-0198, Japan. neurons but also by the timing of the spikes with right-side targeting trials. Notably, we identified
*Corresponding author. Email: fujisawa@brain.riken.jp respect to the phase of the underlying theta os- 51 of 1244 units in the opposite-side rule task

Danjo et al., Science 359, 213–218 (2018) 12 January 2018 1 of 6


R ES E A RC H | R E PO R T

Side arms Other’s normalized rate map


Left Right

1
Center arm
reward reward
spouts spouts

cell number
Left Right

Self Other Start arms

1298
Other 11.5 Self 5.4 Other 16.9 Self 21.1 Other 13.4 Self 26.4 Other 27.3 Self 27.7 L R L R
Start Center Arm Side Arms

Self’s normalized rate map

1
cell number

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Other Other Other Other
Firing rate (Hz)

1298
30
8 15 8
10 20 Significant area on the other’s positions
4 4

1
5 10
0 0 0 0
17.4 d0422_u95 43.9 d0222_u5 17.9 d0330_u74 29.0 d1008_u13

cell number
R

R
Self’s position
L

L
Center

Center

Center

Center
L R

L R

L R

L R

L R Center L R L R Center L R L R Center L R L R Center L R 1298


start arms side arms start arms side arms start arms side arms start arms side arms
Other’s position Other’s position Other’s position Other’s position L R L R
Start Center Arm Side Arms

Firing Rate (Hz) Firing Rate (Hz) Firing Rate (Hz)


Self 26.7 6 Self 14.8 2 Self 10.6 3
0 0 0 15
p<0.01
Number of Units

Theta Phase (degree) Theta Phase (degree) Theta Phase (degree)


360 360 360
10
180 180 180
5
0 0 0
Firing Rate (Hz) Firing Rate (Hz) Firing Rate (Hz)
Other Other 15 Other 0
25.4 20 15.7 12.5 10 0 0.1 0.2 0.3 0.4 0.5
0 0 0 Correlation of
Theta Phase (degree) Theta Phase (degree) Theta Phase (degree) Theta Phase and Other’s Position
360 360 360

180 180 180

d1008_u13 0 d0215_u13 0 d0222_u28 0 start


start T-cross start T-cross T-cross
Position of Rats Position of Rats Position of Rats

Fig. 1. Joint spatial representations of self and other in the horizontal and vertical axes, respectively. The maximum firing rate is
observational task. (A) Schematic of the opposite-side rule. See indicated at the top of each map. (G to I) Linearized and normalized rate
fig. S1A. (B) Schematic of linearizing the trajectories on the T-maze. maps based on the other’s position (G), the self’s position (H), and the
See figs. S3 and S4. (C to F) Units whose firing rates significantly significant area on the other’s position (I), sorted by maximum rate
depended on the other’s position. (Top) Other’s (left) and self’s (right) positions on the other’s map (n = 1298 units). (J to L) Units with
rate maps. (Second from top) Trajectory plots of other (left) and theta-phase precession based on the other’s position. (Top) Self’s rate
self (right). Gray lines, rats’ trajectories; red dots, spike positions. maps (left), linearized rate plots, and theta phases of the spikes as a
(Third from top) Linearized rate plots on other’s position (black lines). function of self’s position (right). (Bottom) Other’s rate maps (left),
Red lines indicate statistically significant bands (P < 0.05) (see fig. S5). linearized rate plots, and theta phases of the spikes as a function of other’s
Blue thick line indicates the significant area. (Bottom) Joint rate position (right). (M) Correlation between theta phase and the other’s
maps. Other’s and self’s linearized positions are coordinated in position. Color bars indicate significant correlation (P < 0.01; n = 59 units).

Danjo et al., Science 359, 213–218 (2018) 12 January 2018 2 of 6


R ES E A RC H | R E PO R T

that had trajectory-specific common place fields reconstructed other’s trajectories revealed that these spikes contained more information about
(Fig. 3, F and G; fig. S11; and SM), which was the spikes of joint-place-cell ensembles contained the other’s place than that obtained by distribu-
significantly higher than the number expected sufficient information regarding the other’s po- tions of time spent in the positional relationships
by chance (P < 0.05) (see SM). sitions (Fig. 4A and fig. S12A). Although the er- of the self and the other. We computed a control
Because the allocentric representation of self’s ror distances between the actual and decoded estimation of the other’s positions by reconstruct-
place was also demonstrated by reliable recon- positions were larger for the other’s decoding ing the self’s positions and then accordingly
struction of self’s positions only from the spikes than those for the self, the differences in the referring to the probability distributions of the
of place-cell ensembles (27, 28), we further tested error distances were as small as 5 cm per time positional relationships (fig. S12B and SM). For
whether the spikes of joint-place-cell ensembles window (200 ms) in both rules (other’s versus the Bayesian reconstructions in this analysis,
could also reconstruct the other’s positions. First, self’s error distances, 20.3 versus 16.1 cm in the the prior templates were computed from trials
we performed Bayesian decoding analysis with opposite-side rule, 20.1 versus 15.1 cm in the same- including both rules, and results were examined
a leave-one-out strategy in each rule (SM). The side rule) (Fig. 4B). We then examined whether based on error distances in a block-wise manner

Fig. 2. Spatial representa- Opposite-side rule Same-side rule Other-preferred cells Goal-preferred cells
(Prospective Cells)
tions of other-preferred
Opposite-side Same-side Opposite-side Same-side
and goal-preferred cells. Other rule rule rule rule
Other
(A) Schematic of the relation-

place field
Other’s
ship of the other’s position
Other Other
and the self’s goal in opposite-

Downloaded from http://science.sciencemag.org/ on February 16, 2018


side and same-side rules.
(B) Schematic explaining
Self Self
other-preferred cells (left)

Self’s goal
and goal-preferred cells
(right). Other-preferred
cells fire preferentially when Self Self

the other is on the same side, Other-preferred cells


regardless of the rule. Simi-
Opposite-side rule Same-side rule Opposite-side rule Same-side rule Opposite-side rule Same-side rule
larly, goal-preferred
cells fire when the self’s Other
goal is on the same side.
(C to E) Rate maps of
other-preferred cells.
(Top) Other’s rate maps
in the opposite-side rule 10.4 14.6 32.5 6.1 29.4 40.6
(left) and same-side rule
Self
(right). (Bottom) Self’s rate
maps in the opposite-side
rule (left) and the same-side
rule (right). See fig. S9
for statistical methods. 14.2 17.9 39.2 12.4 40.5 53.6
(F) Summary of other- d0215_u35 d0330_u70 d0401_u77
preferred cells and goal-
Other-preferred cells
preferred cells (n = total Opposite-side rule Same-side rule
434 units). (G) Linearized
1

Other-preferred cells
and normalized rate
58 cell number

58 (13%)
maps of other-referred Goal-preferred cells
cells, sorted by peak rate 252 (58%)
positions. (H) Other’s (top)
The rest
and self’s (bottom) rate maps 124 (29%)
L R L R L R L R
of goal-preferred cells in the Start Center Arm Side Arms Start Center Arm Side Arms
opposite-side rule (left)
and the same-side rule Goal-preferred cells
(right). (I) Linearized and Opposite-side rule Same-side rule Opposite-side rule Same-side rule
1

normalized other’s rate Other


maps of goal-preferred cells
in the opposite-side task
cell number

(left) and same-side task


(right), sorted by the
maximum rate positions. 22.8 8.4
Self
252

L R L R L R L R
27.5 9.7 Start Center Arm Side Arms Start Center Arm Side Arms
d0215_u32

Danjo et al., Science 359, 213–218 (2018) 12 January 2018 3 of 6


R ES E A RC H | R E PO R T

(Fig. 4, C and D, and SM). Reconstructing trajec- We propose an extended model of hippocam- natorial representations of spatial information
tories without rule information apparently made pal spatial representations that can include di- of self and nonself would open the door to exam-
the error distances of the other’s decoded posi- mensions for both self and other (fig. S13). Our ining whether this allocentric spatial represen-
tions larger, but they were significantly smaller model, encompassing various types of spatial tation extends more generally to other nonliving
than the control estimate of the other’s positions representations, can categorize spatial represen- moving objects (31–33) and how it is generated
(Fig. 4D). The overall averages of the error dis- tations into four types: own place fields, joint in the hippocampal-entorhinal cortex network.
tances of the other’s decoding were less than place fields, other’s place fields, and common Our data indicate that the place cells in the hip-
40 cm and also were significantly smaller than place fields (fig. S13, A to D). In particular, the pocampus encode sufficient spatial information
those of the control estimation in both rules common place field could be hypothesized to be for organizing the recognition of other animals,
(Fig. 4E). a mirror representation of place (29, 30). Combi- which is essential for social behavior (34, 35).

Other 27.2 Self 33.6 2D products Normalized firing rate 1D Products


Other Self
1 1 0.5
X

Normalized firing rate (Hz)


0 0 0

1D Product
1 1
0.76
X 0.5

Downloaded from http://science.sciencemag.org/ on February 16, 2018


d0323_u1
0 0 0

Other 16.3 Self 16.0 2D products


1 1
X 0.5
0 0 0
start T-cross start T-cross start T-cross

Other’s rate maps Self’s rate maps 1D products


1

0.84
d0925_u13
Cell number

Other 19.3 Self 23.4 2D products


45

0.64
L R L R L R L R L R L R
d0213_u26 Start Center Side Start Center Side Start Center Side

Whole 17.2 Right trials Left trials 2D products Whole 13.8 Right trials Left trials 2D products
Other
Other

0.68 0.36

24.1 17.3
Self
Self

0.29 0.89
d0214_58 d0923_32

Fig. 3. Common place fields in self’s and other’s rate maps. (A to C) with common place fields aligned by the position with the maximum
Common place fields of representative units in the other’s (left) and value of the products (n = 45 of 908 units). (F and G) Trajectory-specific
the self’s (middle) rate maps. (Right) The products (element-wise common place fields of two representative units. (Left) Other’s (top) and
multiplications) of normalized other’s and self’s firing rates in each pixel. self’s (bottom) rate maps of whole trials. (Middle) Rate maps with the left and
(D) Linearized other’s (left) and self’s (middle) firing rates and their right trials separated. (Right) The products of normalized other’s and self’s
products (right). The products are the element-wise multiplications of the firing rates of right (top) and left (bottom) targeting trials in each pixel.
normalized firing rates of the self and the other at each position, of the Arrows indicate the centers of common place fields. The maximum color
units shown in (A) to (C). This value was used to identify units with value of the product map was set as 0.5, and the values in the product map
common place fields. (E) Linearized and normalized rate maps of units indicate the maximum of the product.

Danjo et al., Science 359, 213–218 (2018) 12 January 2018 4 of 6


R ES E A RC H | R E PO R T

Opposite-side rule
trial 41 trial 42 trial 43 trial 44 trial 45 trial 46

Other’s
Position
decode
actual
trial 41 trial 42 trial 43 trial 44 trial 45 trial 46
decode
actual
Self’s
Position

trial 47 trial 48 trial 49 trial 50 Opposite-side Same-side


rule rule
Other’s 25 25

Error distance (cm)


Position 20 20

15 15
trial 47 trial 48 trial 49 trial 50

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10 10
Self’s
5 5
Position
0 0
r r
he Self he Self
Ot Ot

Opposite-side rule Opposite-side rule Same-side rule


100 60
5

Error distance / Block (cm)


Other’s decoding
80
Error distance (cm)

4 Control estimation
1 2 3
40
60
6
Same-side rule 40
5 20
20
4
12 3 0 0
1 2 3 4 5 6 1 2 3 4 5 6 de ide
6 -si e-lse
Block Block s itee m
po ul Sa ru
Op r

Fig. 4. Decoding other’s and self’s positions from spikes of hippocampal into six blocks. (D) Error distances of reconstructed other’s positions in each
cells. (A) Reconstructed other’s and self’s positions in the opposite-side block. Red bars, distance between the actual and decoded other’s positions.
rule. Red and blue lines, reconstructed other’s and self’s positions, Gray bars, distance between the actual and estimated other’s positions
respectively. Black lines, actual trajectories of the other or self. (B) Mean (n = 22 sessions) (two-way repeated measures analysis of variance: P < 0.001,
error distances between actual and decoded positions (31 and 28 sessions F5 = 83.95 for the opposite-side rule; P < 0.001, F5 = 72.6 for the same-side
from the opposite-side and same-side rules, respectively). (C to E) The rule). (E) Averaged error distances per block (two-tailed paired t test: P <
reconstructions of other’s positions by using prior templates calculated from 0.001, t21 = –10.70 for the opposite-side rule; P < 0.001, t21 = –10.95 for the
trials including both rules. (C) Schematic of the division of other’s trajectories same-side rule). Data are mean ± SEM.

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Danjo et al., Science 359, 213–218 (2018) 12 January 2018 6 of 6


Spatial representations of self and other in the hippocampus
Teruko Danjo, Taro Toyoizumi and Shigeyoshi Fujisawa

Science 359 (6372), 213-218.


DOI: 10.1126/science.aao3898

The representation of others in space


Different sets of neurons encode the spatial position and orientation of an organism. However, social animals
need to know the position of other individuals for social interactions, observational learning, and group navigation.
Surprisingly, very little is known about how the position of other animals is represented in the brain. Danjo et al. and
Omer et al. now report the discovery of a subgroup of neurons in hippocampal area CA1 that encodes the presence of

Downloaded from http://science.sciencemag.org/ on February 16, 2018


conspecifics in rat and bat brains, respectively.
Science, this issue p. 213, p. 218

ARTICLE TOOLS http://science.sciencemag.org/content/359/6372/213

SUPPLEMENTARY http://science.sciencemag.org/content/suppl/2018/01/11/359.6372.213.DC1
MATERIALS

RELATED http://science.sciencemag.org/content/sci/359/6372/218.full
CONTENT

REFERENCES This article cites 40 articles, 9 of which you can access for free
http://science.sciencemag.org/content/359/6372/213#BIBL

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