Under What Conditions Is Recognition Spared Relative
to Recall After Selective Hippocampal Damage
in Humans?
J.S. Holdstock,
1
*
A.R. Mayes,
1
N. Roberts,
3
E. Cezayirli,
3
C.L. Isaac,
2
R.C. O’Reilly,
4
and K.A. Norman
4
1
Department of Psychology, University of Liverpool,
Liverpool, UK
2
Section of Clinical Neurology, Division of Clinical
Sciences, University of Sheffield, Royal Hallamshire
Hospital, Sheffield, UK
3
Magnetic Resonance and Image Analysis Research
Centre, University of Liverpool, Liverpool, UK
4
Department of Psychology, University of Colorado,
Boulder, Colorado
ABSTRACT: The claim that recognition memory is spared relative to
recall after focal hippocampal damage has been disputed in the literature.
We examined this claim by investigating object and object–location recall
and recognition memory in a patient, YR, who has adult-onset selective
hippocampal damage. Our aim was to identify the conditions under which
recognition was spared relative to recall in this patient. She showed
unimpaired forced-choice object recognition but clearly impaired recall,
even when her control subjects found the object recognition task to be
numerically harder than the object recall task. However, on two other
recognition tests, YR’s performance was not relatively spared. First, she
was clearly impaired at an equivalently difficult yes/no object recognition
task, but only when targets and foils were very similar. Second, YR was
clearly impaired at forced-choice recognition of object–location associa-
tions. This impairment was also unrelated to difficulty because this task
was no more difficult than the forced-choice object recognition task for
control subjects. The clear impairment of yes/no, but not of forced-
choice, object recognition after focal hippocampal damage, when targets
and foils are very similar, is predicted by the neural network-based
Complementary Learning Systems model of recognition. This model pos-
tulates that recognition is mediated by hippocampally dependent recol-
lection and cortically dependent familiarity; thus hippocampal damage
should not impair item familiarity. The model postulates that familiarity is
ineffective when very similar targets and foils are shown one at a time and
subjects have to identify which items are old (yes/no recognition). In
contrast, familiarity is effective in discriminating which of similar targets
and foils, seen together, is old (forced-choice recognition). Independent
evidence from the remember/know procedure also indicates that YR’s
familiarity is normal. The Complementary Learning Systems model can
also accommodate the clear impairment of forced-
choice object–location recognition memory if it incor-
porates the view that the most complete convergence
of spatial and object information, represented in differ-
ent cortical regions, occurs in the hippocampus.
Hippocampus 2002;12:341–351.
© 2002 Wiley-Liss, Inc.
INTRODUCTION
One influential view concerning the role of the hip-
pocampus in memory is that it is critically involved in
both recall and recognition (Reed and Squire, 1997;
Squire and Zola, 1998). This view therefore predicts that
both types of memory will be impaired equally by selec-
tive hippocampal damage if tests are matched for diffi-
culty.
An alternative view is that, although critical for recall,
the hippocampus is not required for recognition memory
decisions that can be made successfully on the basis of the
familiarity of the material (Aggleton and Shaw, 1996;
Aggleton and Brown, 1999). This proposed dissociation
has received some support from a recent functional mag-
netic resonance imaging (MRI) study (Eldridge et al.,
2000). This study used the remember/know procedure to
tap recollection and familiarity, respectively, of recently
studied words. It found that hippocampal activation, rel-
ative to a prestimulus baseline in which subjects fixated a
cross-wire, was greater during remember responses than
during know responses. However, evidence that know
responding, and therefore familiarity, does not involve
Grant sponsor: Medical Research Council of the United Kingdom; Grant
number: G9300193.
*Correspondence to: J.S. Holdstock, Department of Psychology, University
of Liverpool, Eleanor Rathbone Building, P.O. Box 147, Liverpool, L69
3BS, UK. E-mail: j.holdstock@liverpool.ac.uk
Accepted for publication 24 August 2001
DOI 10.1002/hipo.10011
Published online 00 Month 2001in Wiley InterScience (www.interscience.
wiley.com).
HIPPOCAMPUS 12:341–351 (2002)
© 2002 WILEY-LISS, INC.