In the Scottish highlands, hikers risk being
caught in a sudden mist that obliterates all
visible landmarks. People in this situation
have two options: attempt to retrace their
steps by estimating how far and in which
direction they have traveled, or wait until the
mist lifts and the landmarks return. The
neural basis of these spatial abilities in
humans is not clear. In rodents, however,
both types of navigation may rely on hip-
pocampal neurons called ‘place cells’
1
, which
encode spatial information defined by self-
motion cues
2,3
or by visual landmarks
4–6
.
One influential theory is that together, the
population of place cells provides a ‘cogni-
tive map’ of an animal’s environment
7
.
In this issue, Rosenzweig et al.
8
compare
these hippocampal cognitive maps and spa-
tial behavior in young adult and aged
rodents. They find that the ability of both
young adult and aged rats to find a reward
in the environment is correlated with the
ability of place cells in the hippocampus to
switch between two different cognitive
maps, one based on self-motion cues that
are irrelevant to solving the task, and
another based on relevant landmark cues.
Intriguingly, they observe that old rats are
impaired relative to young adult rats, both
in switching from the irrelevant to the rele-
vant map and in finding the reward (Fig. 1).
Since the discovery of hippocampal place
cells
1
in the early 1970s, researchers have
sought to understand which aspects of the
environment control their spatial activity.
Early studies demonstrated that the location in
which a place cell fires—its ‘place field’—is
controlled by visual landmarks in the environ-
ment
4–6
. Thus, if one rotates the landmarks in
an environment by 90° while the rat is else-
where, then when the rat returns, its place
fields will also rotate by 90° to agree with the
landmarks. Visual landmarks are not the whole
story, however. Place cells are also controlled by
path integration—deriving the direction and
distance traveled from self-motion informa-
tion, including motor propioception, the
vestibular system and perhaps optic flow
2,3
.
E.R.W. is in the Division of Neuroscience and
Centre for Neuroscience Research, University of
Edinburgh, 1 George Square, Edinburgh, EH8 9JZ,
Scotland. P.A.D. is in the Department of
Psychology, University of Stirling, Stirling FK9 4LA,
Scotland.
e-mail: emma.wood@ed.ac.uk
Aging, spatial behavior and the cognitive map
Emma R Wood & Paul A Dudchenko
Hippocampal neurons are thought to form a cognitive map of the environment based on multiple cues. A new study shows that
young animals switch between cues more easily than aged animals and also perform better on a spatial learning task.
NEWS AND VIEWS
cells within one or more region of the
brain. The preliminary results of van
Swinderen and Greenspan suggest that
20–30 Hz activity is phase-locked across
regions of the central brain, thus showing
spatiotemporal synchrony or coherence—a
hallmark of early perception in verte-
brates
9
. Increases in power within the
20–30 Hz bandwidth may reflect changes in
the recruitment, firing rate and synchrony
of a subpopulation of cells within the
medial protocerebrum or an adjacent
region. Future experiments using micro-
arrays of extracellular electrodes combin-
ed, when possible, with intracellular
recordings, should be able to test these
various hypotheses.
Although Drosophila will never win
high marks as an electrophysiological
model, it does permit extraordinarily pre-
cise manipulations of gene expression in
both time and space. In particular, by
clever implementation of the GAL4/UAS
expression system of yeast
10
, it is possible
to express a gene of interest (including
ones not found in the fly’s genome)
ectopically within specific regions of the
nervous system. For example, the gene for
tetanus toxin or an allele of shibire can be
introduced to block synaptic transmis-
sion. Such techniques have been used to
examine mechanisms of sensory discrimi-
nation
11
, sensorimotor integration
12
and
learning and memory
13
. Until now, how-
ever, physiological links between gene
products and behavior have been elu-
sive—especially at the systems level.
By systematically targeting reversible
temperature-sensitive mutations in mem-
brane conductance and synapse function
to specific regions of the brain, van
Swinderen and Greenspan spatially local-
ized the origins of the 20–30 Hz
response—at least in part—to synaptic
output from the mushroom bodies.
Biochemical, physiological and behavioral
evidence implicates these structures in
odor-mediated learning in flies
14
. It
remains to be shown how visual feedback
is integrated with mushroom body out-
put. Postsynaptic targets of mushroom
body efferents such as those within the
lateral horn are probably involved
15
.
The discovery of structure–function
relationships mediating higher-order
brain processes such as perception, atten-
tion and learning will be accelerated by
integrating molecular-genetic, physiologi-
cal and behavioral approaches. Toward
these ends, the experimental power of cou-
pling spatially localized and reversible
genetic manipulations with robust physio-
logical recording preparations in behaving
flies is difficult to overstate. Armed with a
physiological assay for object salience, the
next challenge is to find out how this sig-
nal is used to structure fly motor behaviors
such as foraging or courtship. Given the
remarkable complexity even within one of
nature’s smaller brains, this challenge is
not an easy one. As Donald Hebb noted,
“the brain…may not be able to do simple
things in a simple way.”
1. van Swinderen, B. & Greenspan, R.G. Nat. Neurosci.
6, 581–588 (2003).
2. Laurent, G. Science 286, 723–728 (1999).
3. Egelhaaf, M. & Kern, R. Curr. Opin. Neurobiol. 12,
699–706 (2002).
4. Trimarchi, J.R., Jin, P. & Murphey, R.K. Intl. Rev.
Neurobiol. 43, 241–264 (1999).
5. Ernst, R. & Heisenberg, M. Vision Res. 39,
3920–3933 (1999).
6. Götz, K.G. Basic Life Sci. 16, 391–407 (1980).
7. Frye, M.A., Tarsitano, M. & Dickinson, M.H. J. Exp.
Biol. 206, 843–855 (2003).
8. Brett, M., Johnsrude, I.S. & Owen, A.M. Nat. Rev.
Neurosci. 3, 243–249 (2002).
9. Singer, W. Nature 397, 391–393 (1999).
10. Brand, A. & Perrimon, N. Development 118,
401–415 (1993).
11.Keller, A., Sweeney, S.T., Zars, T., O'Kane, C.J. &
Heisenberg, M. J. Neurobiol. 50, 221–223 (2002).
12. Strauss, R. Curr. Opin. Neurobiol. 12, 633–638
(2002).
13. deBelle, J.S. & Heisenberg, M. Science 263,
692–695 (1994).
14. Strausfeld, N.J., Hansen, L., Li, Y.S., Gomez, R.S. &
Ito, K. Learn. Mem. 5, 11–37 (1998).
15. Ito, K. et al. Learn. Mem. 5, 52–77 (1998).
546 VOLUME 6 | NUMBER 6 | JUNE 2003 NATURE NEUROSCIENCE
© 2003 Nature Publishing Group http://www.nature.com/natureneuroscience