I would like to correct a statement that was
made by Squire et al. in a recent Review of rec-
ognition memory
1
. On page 879, the Review
1
states that ‘In one study in monkeys
72
, 34%
of hippocampal cells responded differently
depending on whether the stimulus was famil-
iar or novel.’ Reference 72 is a paper by Wilson
et al.
2
: their figure for the number of neurons
that respond differently to novel stimuli (that
is, stimuli that have never previously been pre-
sented or stimuli that have not been seen for
many days) presented for the first time than
to familiar stimuli (stimuli being shown for
the second time in a brief period) is zero out
of >650 neurons recorded in the hippocampus
and subicular cortex — that is, 0% (see REF. 2,
page 315).
The figure of 34% actually refers to
repeated presentations of familiar stimuli in
a delayed matching-to-sample task (DMS
task; see REF. 2, page 319). It is important to
understand that these familiar stimuli are
repeated frequently within short time per-
iods and that the response difference being
referred to is that between stimuli being pre-
sented for the second time on match trials and
stimuli being presented for the second time
on non-match trials. Before such response
differences between match and non-match
trials can be accepted as providing a substrate
for general, long-term familiarity discrimina-
tion, evidence must be given that they satisfy
the appropriate criteria. The delay interval
between the first and second stimulus pres-
entations in the experiments referred to was
0.5 seconds — well within the time range of
short-term memory or attentive mechanisms.
Such match–mismatch differences have not
been demonstrated across time delays appro-
priate to long-term memory, when so many
items must be retained that they are outside
the capacity of short-term memory, and when
the delay intervals are filled with distraction.
Other references
3,4,5
cited in the Review
1
also
do not provide such evidence.
Indeed, Wilson et al.
2
provided evidence
that the match–mismatch differences do not
provide a possible general substrate for long-
term familiarity discrimination and are not
related to novelty detection: referring to 395
hippocampal neurons recorded in a serial-
recognition task, they state (on page 318)
that, “For none of these units were consistent
differences found between trials on which
novel stimuli were presented and those on
which the stimuli reappeared as familiar. An
additional >250 units tested with objects and
in the DMS task for stimuli varying in their
novelty/familiarity did not show consistent
responses dependent on the novelty/famili-
arity of the stimuli.” Crucially, agreeing with
these findings, Riches et al.
6
further confirmed
that when novel stimuli were introduced into
such a delayed matching-to-sample task, the
responses of hippocampal neurons did not dif-
ferentiate between stimuli that were novel and
stimuli that were highly familiar. Hence, it is
possible to dissociate responses to novelty from
those to repeated familiar stimuli on match
or mismatch trials in a delayed matching-
to-sample task.
This situation contrasts with findings for
the perirhinal and adjacent cortex. Here, the
responses of up to 25% of the neurons are
reduced when initially novel stimuli are seen
for a second time, regardless of whether the
stimuli are presented in a delayed matching-
to-sample task or in other situations
2,6–12
.
Such response reductions have been shown
to occur when the time delay between pres-
entations is long (~24 hours in many cases),
when the delay interval is filled with distrac-
tions, and when the number of items need-
ing to be held in the memory is well over
the capacity of short-term memory
6,8,12–14
.
Accordingly, such response reductions do
satisfy the criteria of general long-term
familiarity discrimination.
By contrast, when more complex discrimi-
nations of prior occurrence are required, par-
ticularly when subjects are taught to encode
spatial information, hippocampal neurons
are often involved (for example, in monkeys
15
,
rats
5,16
and humans
17
). It is unsurprising that
the perirhinal cortex and the hippocampus
work cooperatively when it is appropriate
— this does not prevent their different func-
tions from being dissociated under other
circumstances
2,6,12–14,16
.
University of Bristol, MRC Centre for Synaptic
Plasticity, Department of Anatomy, School of Medical
Sciences, Bristol, BS8 1TD, UK.
e-mail: M.W.Brown@bristol.ac.uk
doi:10.1038/nrn2154-c1
Published online 2 April 2008
1. Squire, L. R., Wixted, J. T. & Clark, R. E. Recognition
memory and the medial temporal lobe: a new
perspective. Nature Rev. Neurosci. 8, 872–883 (2007).
2. Wilson, F. A. W., Brown, M. W. & Riches, I. P. in
Cellular Mechanisms of Conditioning and Behavioral
Plasticity (eds Woody, C. D. Alkon, D. L. & McGaugh,
J. L.) 313–328 (Plenum, New York, 1988).
3. Otto, T. & Eichenbaum, H. Neuronal activity in the
hippocampus during delayed non-match to sample
performance in rats: evidence for hippocampal
processing in recognition memory. Hippocampus 2,
323–334 (1992).
4. Suzuki, W. A. & Eichenbaum, H. The neurophysiology
of memory. Ann. NY Acad. Sci. 911, 175–191 (2000).
5. Wood, E. R., Dudchenko, P. A. & Eichenbaum, H.
The global record of memory in hippocampal neuronal
activity. Nature 397, 613–616 (1999).
6. Riches, I. P., Wilson, F. A. W. & Brown, M. W. The
effects of visual stimulation and memory on neurons of
the hippocampal formation and the neighboring
parahippocampal gyrus and inferior temporal cortex
of the primate. J. Neurosci. 11, 1763–1779 (1991).
7. Brown, M. W., Wilson, F. A. W. & Riches, I. P. Neuronal
evidence that inferomedial temporal cortex is more
important than hippocampus in certain processes
underlying recognition memory. Brain Res. 409,
158–162 (1987).
8. Fahy, F. L., Riches, I. P. & Brown, M. W. Neuronal
activity related to visual recognition memory: long-
term memory and the encoding of recency and
familiarity information in the primate anterior and
medial inferior temporal and rhinal cortex. Exp. Brain
Res. 96, 457–472 (1993).
9. Li, L., Miller, E. K. & Desimone, R. The representation
of stimulus familiarity in anterior inferior temporal
cortex. J. Neurophysiol. 69, 1918–1929 (1993).
10. Miller, E. K., Li, L. & Desimone, R. Activity of neurons
in anterior inferior temporal cortex during a short-
term memory task. J. Neurosci. 13, 1460–1478
(1993).
11. Sobotka, S. & Ringo, J. L. Investigation of long-term
recognition and association memory in unit responses
from inferotemporal cortex. Exp. Brain Res. 96,
28–38 (1993).
12. Xiang, J. Z. & Brown, M. W. Differential neuronal
encoding of novelty, familiarity and recency in regions
of the anterior temporal lobe. Neuropharmacology
37, 657–676 (1998).
13. Brown, M. W. & Aggleton, J. P. Recognition memory:
what are the roles of the perirhinal cortex and
hippocampus? Nature Rev. Neurosci. 2, 51–61 (2001).
14. Brown, M. W. & Xiang, J. Z. Recognition memory:
neuronal substrates of the judgement of prior
occurrence. Prog. Neurobiol. 55, 149–189 (1998).
15. Rolls, E. T. et al. Hippocampal neurons in the monkey
with activity related to the place in which a stimulus is
shown. J. Neurosci. 9, 1835–1845 (1989).
16. Wan, H., Aggleton, J. P. & Brown, M. W. Different
contributions of the hippocampus and perirhinal
cortex to recognition memory. J. Neurosci. 19,
1142–1148 (1999).
17. Rutishauser, U., Namelak, A. N. & Schuman, E. M.
Single-trial learning of novel stimuli by individual
neurons of the human hippocampus-amygdala
complex. Neuron 49, 805–813 (2006).
Hippocampal and perirhinal
functions in recognition memory
Malcolm W. Brown.
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