function of hippocampus

[David Redish]

Ken Miller wrote:

>With respect to recent postings about models of hippocampus and
>memory, I'd like to toss in a cautionary note.  A recent report
>(Elisabeth A. Murray and Mortimer Mishkin, "Object Recognition and
>Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala
>and Hippocampus", J. Neuroscience, August 15, 1998, 18(16):6568-6582)
>finds no deficit in tasks involving visual recognition memory or
>spatial memory with lesions of hippocampus and amygdala.  Instead,
>deficits in both cases are associated with, and only with, lesion of
>the overlying rhinal cortex.  They mention in the discussion evidence
>that "has suggested that the hippocampus may be more important for
>path integration on the basis of self-motion cues than for location
>memory, per se" (though Redish' recent posting mentions evidence
>against this from recent experiments of Alyan and McNaughton; I
>couldn't find a reference in medline).  This is the latest in a series
>of reports along these lines from the Mishkin lab, who did much of the
>original lesion work that seemed to implicate hippocampus in memory.
>
>I'm not in any way an expert on this literature -- only a very distant
>observer -- but I worry that, based on lesion studies that also
>involved lesions of overlying cortex, both the neuroscience and
>connectionists communities may have jumped to a wrong conclusion that
>the hippocampus has a special role in episodic and/or spatial memory.
>I'd be interested to know if there's still good reason to believe in
>such a role ...

One should be very careful about taking anything in the primate
literature as bearing on spatial navigation.  All of the primate
hippocampal recordings and all primate hippocampal lesions studies
have used primates looking at a constellation of objects or being
moved about the room in chairs.  Rodent studies have shown that
hippocampal lesions affect environmental dependent tasks much more so
than object dependent tasks (see, for example, Cassaday and Rawlins,
1997).  Also, rats restrained by towels or laying in hammocks and
passively moved around the room do not show normal place fields
(Foster et al. 1989, Gavrilov et al. 1996).

The specific task used by Murray and Mishkin (1998) was to find food
from one of two wells placed in front of the animal.  This task is not
"spatial navigation"; it is spatial reasoning.  Major distinctions can
be drawn between this task and the kind of hippocampal-dependent tasks
used in rodent navigation.  (1) The task can be solved by an
egocentric spatial reasoning system, while the rodent hippocampus
seems to be critically involved in allocentric spatial reasoning.  (2)
The task is dependent on small objects in front of the animal, while
the rodent navigation tasks dependent on the hippocampus require
manipulations of environmental context.

But there is another very nice result from Murray and Mishkin (1996)
that does bear on this issue: Alvarez et al. (1994) tested primates
with hippocampal lesions in a delayed-non-match-to-sample task (DNMS).
Alvarez et al. found that their hippocampally lesioned animals were
impaired at long delays (10 minutes and 40 minutes), but not short
delays (8 sec, 40 sec, 1 minute).  They interpreted this difference as
a consequence of the length of the delay.  However, they did not use
the same experimental paradigm for the short and long delay trials:
for the longer trials, they removed the monkey from the apparatus, put
it back in its home cage during the delay, and returned it to the
apparatus after the delay.  If the hippocampus is critical for the
reinstantiation of context on returning to an environment, we might
expect this removal from the environment to strongly affect the
hippocampally lesioned animals (Nadel, 1995, Redish, 1997).  Murray
and Mishkin (1996) tested exactly this: they used a
continuous-non-match-to-sample task (CNMS) which is similar to the
DNMS task except that animals are shown a sequence of example objects
and then shown novel pairs in reverse order.  This means that although
there is a delay between the time the animal sees the first object and
when it sees the corresponding last pair, the animal never leaves the
experimental situation.  Murray and Mishkin showed that if the animals
do not leave the context, then they can perform the task well even
without a hippocampus.  This environmental context-change is, I think,
a better analogy to the rodent navigation literature.

adr

PS. The Alyan et al. 1997 reference is to a neuroscience abstract.  I
don't know the current status of the paper they are writing based on
that work.

REFERENCES

P. Alvarez and L. R. Squire (1994) Memory consolidation and the medial
temporal lobe: A simple network model, Proceedings of the National
Academy of Sciences, USA, 91:7041-7045.

H. J. Cassaday and J. N. P. Rawlins (1997) The hippocampus, objects,
and their contexts, Behavioral Neuroscience, 111(6):1228-1244.

T. C. Foster, C. A. Castro and B. L. McNaughton (1989) Spatial
selectivity of rat hippocampal neurons: Dependence on preparedness
for movement, Science, 244:1580-1582.

V. V. Gavrilov, S. I. Wiener and A. Berthoz (1996) Discharge correlates of
hippocampal neurons in rats passively displaced on a mobile robot,
Society for Neuroscience Abstracts, 22:910.

E. A. Murray and M. Mishkin (1996) 40-minute visual recognition memory
in rhesus monkeys with hippocampal lesions, Society for Neuroscience
Abstracts, 22:281.

L. Nadel, The role of the hippocampus in declarative memory: A
commentary on Zola-Morgan, Squire, and Ramus, 1994, Hippocampus,
5:232-234.

A. D. Redish (1997) Beyond the Cognitive Map: Contributions to a
Computational Neuroscience Theory of Rodent Navigation.  PhD
Thesis. Carnegie Mellon University.

S. Zola-Morgan and L. R. Squire and S. J. Ramus (1994) Severity of
memory impairment in monkeys as a function of locus and extent of
damage within the medial temporal lobe memory system, 4:483-495.