HIPPOCAMPUS 23:873878 (2013)
Dopamine D1 Receptor Activity Modulates Object Recognition
Memory Consolidation in the Perirhinal Cortex But Not in the
Hippocampus
Israela Balderas, Perla Moreno-Castilla, and Federico Bermudez-Rattoni*
ABSTRACT: It has been proposed that distributed neuronal networks
in the medial temporal lobe process different characteristics of a recog-
nition event; the hippocampus has been associated with contextual rec-
ollection while the perirhinal cortex has been linked with familiarity.
Here we show that D1 dopamine receptor activity in these two struc-
tures participates differentially in object recognition memory consolida-
tion. The D1 receptor antagonist SCH23390 was infused bilaterally 15
min before a 5 min sample phase in either rats perirhinal cortex or dor-
sal hippocampus, and they were tested 90 min for short-term memory
or 24 h later for long-term memory. SCH23390 impaired long-term
memory when infused in the perirhinal cortex but not when infused in
the hippocampus. Conversely, when the D1 receptor agonist SKF38393
was infused 10 min before a 3 min sample phase in the perirhinal
cortex, long-term memory was enhanced, however, this was not
observed when the D1 agonist was infused in the hippocampus. Short-
term memory was spared when SCH23390 or SKF38393 were infused
in the perirhinal cortex or the dorsal hippocampus suggesting that
acquisition was unaffected. These results suggest that dopaminergic
transmission in these medial temporal lobe structures have a differential
involvement in object recognition memory consolidation. V C 2013 Wiley
Periodicals, Inc.
KEY WORDS: medial temporal lobe; memory modulation;
SCH23390; SKF38393; D1 receptors
INTRODUCTION
Recognition memory is a fundamental facet of our ability to remem-
ber. This process has been described as the ability to know whether or
not something has been previously experienced [individual stimulus or a
whole event (Mandler, 1980; Brown and Aggleton, 2001)]. The partici-
pation of the perirhinal cortex (PRH) and hippocampus (HIP) in this
type of memory has been extensively studied. A current debate is whether
the PRH and the HIP participate differentially or not in the
n de Neurociencias, Instituto de Fisiologa Celular, Universidad
Divisio
Nacional Auto noma de Mexico, Apartado Postal 70-253, 04510, Mexico
D.F, Mexico
Grant sponsor: CONACYT; grant number: 155242; Grant sponsor:
DGAPA-UNAM; grant number: IN216709.
*Correspondence to: Federico Bermudez-Rattoni, Divisi on de Neurocien-
cias, Instituto de Fisiologa Celular, Universidad Nacional Autonoma
de Mexico, A.P. 70-253 Mexico D.F., 04510 Mexico. E-mail:
fbermude@ifc.unam.mx
Accepted for publication 7 May 2013.
DOI 10.1002/hipo.22143
Published online 11 June 2013 in Wiley Online Library
(wileyonlinelibrary.com).
C 2013 WILEY PERIODICALS, INC.
V
familiarization processing, as well as the recollection
component of recognition memory (Brown and Aggle-
ton, 2001; Yonelinas et al., 2002; Smith et al., 2011;
Song et al., 2011). There is experimental evidence sup-
porting both views. Several groups claim that the HIP
is specifically involved in recollection, while familiar-
ization depends on the PRH (Brown and Aggleton,
2001; Eichenbaum et al., 2007). An opposing view
sustains that both the PRH and the HIP are involved
in familiarity and recollection (Rossato et al., 2007;
Squire et al., 2007; Myskiw et al., 2008; Diana and
Ranganath, 2011; Wixted and Squire, 2011).
We have reported a significant increase in the release
of dopamine in rodents insular cortex during the pre-
sentation of novel stimuli (i.e., objects or tastes); while
the release of dopamine remained unchanged in the
hippocampus (Guzman-Ramos et al., 2012), suggest-
ing a dissociative involvement of dopaminergic trans-
mission in cortical familiarity-based recognition.
Several studies using systemic administrations of dopa-
mine receptors agonists/antagonists have related the
D1 dopamine receptor activity with object recognition
memory (Besheer et al., 1999; de Lima et al., 2011).
Even though the PRH and the HIP are two structures
closely related to recognition memory, the role of
dopamine activity in these structures had not been
addressed.
The aim of this study was to evaluate the participa-
tion of D1 receptors activity in the PRH and the
HIP. We infused the D1 antagonist SCH23390 or the
D1 agonist SKF38393 in to the PRH or the HIP and
tested the rats to short (STM, 90 min) or long-term
(LTM, 24 h) memory on object recognition task.
Since it has been described that release of dopamine
significantly increased during the presentation of novel
objects in ORM sample phase (Guzman-Ramos et al.,
2012), we infused the drugs before the presentation
of novel stimuli in order to manipulate the receptors
during the dopamine release.
To determine whether D1 receptors activity plays a
role in object recognition memory at short or long
delays, we infused either vehicle or SCH23390 into
the PRH or the HIP 15 min before the sample (Guz-
man-Ramos et al., 2010); and the animals were tested
90 min or 24 h after sample phase (see Figs. 1a,d).
All experiments described in this study were carried
out in independent groups.
874 BALDERAS ET AL.
FIGURE 1. The D1 receptor antagonist SCH23390 disrupted
ORM consolidation when infused in the PRH but not in the HIP.
Recognition indexes are shown for the sample and test phases. A
recognition index equal to 0.5 means no preference for any object
(dotted line). An index higher than 0.5 indicates preference for
that object. Schematic representation of the behavioral protocol.
On the sample phase, rats were exposed to two identical objects
(A-A) for 5 min, and a memory test was conducted 90 min (a) or
24 h (d) after the end of the sample phase, in which a copy of the
familiar object (A) and a new one (B) were presented. The groups
The groups infused into the PRH or the HIP exhibited a simi-
lar amount of time exploring each one of the two identical
objects in the sample phase (see Figs 1b,c, for STM 1e and f, for
LTM). One-sample t-tests showed no preference for any object
for all the groups; for STM groups: PRH-VEH (P 5 0.97),
PRH-SCH23390 (P 5 0.77), HIP-VEH (P 5 0.74), HIP-
SCH23390 (P 5 0.93); and for LTM groups: PRH-VEH
(P 5 0.63), PRH-SCH23390 (P 5 0.66), HIP-VEH (P 5 0.81),
and HIP-SCH23390 (P 5 0.29).
On STM test (90 min after sample phase) all the groups were
infused with vehicle or SCH23390 into PRH or the HIP
explored more the novel object. One-sample t-tests showed that
the preference for the novel objects was different from chance
level for all groups [PRH-VEH (P < 0.02), PRH-SCH23390
(P < 0.02), HIP-VEH (P < 0.01), HIP-SCH23390 (P < 0.001);
see Figs. 1b,c, test phase]. Two-way ANOVA did not reveal sig-
nificant effects of drug [F(1,27)5 0.010, P 5 0.92], structure
[F(1,27)5 1.24, P 5 0,27], or drug by structure interaction
[F(1,27)5 0.01, P 5 0.91]. These results indicated that D1 dopa-
mine receptor activity in the PRH or in the HIP did not play a
role in object recognition memory at short delays and showed
that rats were able to acquire the information about objects in
presence of the antagonist.
On LTM test (24 h), rats infused in the PRH or the HIP with
vehicle solution showed significant preference for the novel
Hippocampus
infused 15 min before the sample phase with SCH23390 into the
PRH (b), or HIP (c) showed a high recognition index for the
novel object on STM test. One sample t-tests showed that prefer-
ence for the novel objects was different from chance level.
SCH23390 disrupted LTM when infused into the PRH (e), but
not when infused into the HIP (f ). One sample t-test showed that
preference for the novel object was not different from chance level
only for the group infused with SCH23390 into PRH (P 5 NS).
*P < 0.05, **P < 0.01, vs. recognition index 5 0.5.
object. SCH23390 infused in the PRH disrupted the preference
for the novel object on test phase. However, SCH23390 infu-
sions in the HIP did not impair the preference for the novel
object. Two-way ANOVA reveal a significant effects of drug
[F(1,42)5 4.7, P 5 0.03], but no significant effects of structure
[F(1,42)5 1.92, P 5 0.17], or drug by structure interaction
[F(1,42)5 1.93, P 5 0.17]. An unpaired t-test indicated differen-
ces between treatments (vehicle vs. SCH23390) for the PRH
(t(29)5 2.31, P < 0.03) but not for the HIP (t(14)5 0.53,
P 5 0.60). Furthermore, a one-sample t-tests showed that prefer-
ence for the novel objects was different from chance level in all
groups PRH-VEH (P < 0.001), HIP-VEH (P < 0.001), HIP-
SCH23390 (P 5 0.01), except when SCH23390 was infused in
the PRH (PRH-SCH23390: P 5 0.25) (see Figs. 1e,f, test
phase). These results suggest that the D1 receptor antagonist
SCH23390 disrupted ORM consolidation when infused in the
PRH but not in the HIP.
Since object recognition memory consolidation was
disrupted by infusion of the D1 receptor antagonist in the
PRH, we next sought to determine whether activation of these
receptors could enhance memory consolidation. To test this,
we performed vehicle or SKF38393 infusions in the PRH or
in the HIP 10 min before the sample phase (Hotte et al.,
2005) and memory was tested 90 min or 24 h later (see
Figs. 2a,d).
 D1 RECEPTOR MODULATES RECOGNITION MEMORY CONSOLIDATION
FIGURE 2. The D1 dopamine receptor agonist SKF38393
enhanced ORM consolidation when infused into the PRH but not
in to HIP. Recognition indexes are as shown in Figure 1. On the
sample phase, rats were exposed to two identical objects (A-A) for
3 min, and a memory test was conducted 90 min (a) or 24 h (d)
after the end of the sample phase, in which a copy of the familiar
object (A) and a new one (B) were presented. The groups infused
10 min before the sample phase with SKF38393 into the PRH
(b), or HIP (c) showed a high recognition index for the novel
For the following experiments sample phase lasted 3 min
instead of 5 min because control behavioral experiments
showed that object recognition memory lasted in the long term
with five but not three minutes of sample phase (see Fig. 3).
The groups infused into the PRH or the HIP exhibited a simi-
lar amount of time exploring each one of the two identical
objects in the sample phase (see Figs. 2b,c, for STM and Figs.
2e,f, for LTM). One-sample t-tests showed no preference for
any object for all the groups; for STM groups: PRH-VEH
(P 5 0.88), PRH-SKF38393 (P 5 0.17), HIP-VEH (P 5 0.37)
and HIP- SKF38393 (P 5 0.52); and for LTM groups: PRH-
VEH (P 5 0.37), PRH- SKF38393 (P 5 0.53), HIP-VEH
(P 5 0.82) and HIP- SKF38393 (P 5 0.23).
On STM test (90 min) all groups, the infused with vehicle
or with SKF38393 in the PRH or the HIP explored more the
novel object. One-sample t-tests showed that preference for the
novel object was different from chance level in all groups
[PRH-VEH (P < 0.0005), PRH- SKF38393 (P < 0.003), HIP-
VEH (P < 0.009), HIP- SKF38393 (P < 0.002); see Figs. 2b,c,
test phase]. Two-way ANOVA did not reveal significant effects
of drug [F(1,26)5 0.005, P 5 0.94], structure [F(1,26)5 0.50,
P 5 0.48] or drug by structure interaction [F(1,26)5 2.1,
P 5 0.16]. These results indicate that activation of D1 dopa-
mine receptor by the agonist SKF38393 in the PRH or in the
875
object on STM test. One sample t-tests showed that preference for
the novel objects was different from chance level. (e) The group
infused into the PRH showed a high recognition index for the
novel object on the LTM test. While the group infused into the
HIP (f ) showed a low recognition index. One-sample t tests
showed that preference for the novel object was different from
chance level only for PRH infused group. *P < 0.05, **P < 0.01, vs.
recognition index 5 0.5.
HIP did not affect object recognition memory at short delays
and show that rats were able to acquire the information about
objects in presence of the agonist.
On LTM test (24 h), rats infused in the PRH or the HIP
with vehicle solution did not show significant preference for
the novel object. Figures 2e,f, also showed that SKF38393
infused into the HIP did not affect the discrimination between
familiar and novel objects (Fig. 2f, test phase). However,
SKF38393 infusions in the PRH enhanced the preference of
the rats for the novel object (Fig. 2e, test phase). Two-
way ANOVA reveal a significant effects of structure [F(1,29)5
8.6, P 5 0.006], no significant drug effect [F(1,29)5 0.36,
P 5 0.56] but a significant drug by structure interaction
[F(1,29)5 4.62, P < 0.04]. Fishers post hoc test revealed that
the group infused with SKF38393 into the PRH was different
from the other groups (ps<0.05). A one-sample t-tests showed
that preference for the novel objects was not different from
chance level in all groups PRH-VEH (P 5 0.44), HIP-VEH
(P 5 0.96), HIP- SKF38393 (P 5 0.20), except when
SKF38393 was infused in the perirhinal cortex (PRH-
SKF38393: P < 0.002). These results indicate that the D1
dopamine receptor agonist SKF38393 infused into the PRH
but not in the HIP enhances object recognition memory
consolidation.
Hippocampus
876 BALDERAS ET AL.
FIGURE 3. Object recognition memory last longer with 5 but
not 3 minutes of sample phase. Recognition indexes are as in Fig-
ure 1. Schematic representation of the behavioral protocol for 3
min (a,c) or 5 min (e,g) sample phase. The group tested 90 min
(b) after a 3 min sample phase showed a high recognition index
for the novel object on the short-term but not in the long-term
memory test (d). One sample t-tests showed that preference for
novel objects was different from chance level only in the STM
group. The groups tested 90 min (f ) or 24 h (h) after a 5 min
sample phase showed a high recognition index for the novel object
on short and long-term memory test. One sample t-tests showed
that preference for novel objects was different from chance level
for both groups. **P < 0.01, vs. recognition index 5 0.5.
TABLE 1.
Total exploration in seconds 6 SEM (a) STM and (b) LTM with vehicle and SCH23390 infusions. (c) STM and d) LTM with vehicle and
SKF38393 for PRH groups. e) STM and f) LTM with vehicle and SCH23390 infusions; g) STM and h) LTM with vehicle and SKF38393 for HIP
groups. Unpaired t-test showed no differences between groups infused with the drug and its respective vehicle.
Hippocampus
Total exploration time on the sample phase was similar for
PRH and HIP groups (see Table 1). These results suggest that
SCH23390 or SKF38393 infused into the PRH or the HIP
did not disrupt processes such as motor skills or motivation to
explore the objects.
The role of dopamine in memory formation has been exten-
sively described (Lisman et al., 2011). It has been suggested
that D1/D5 receptors might modulate neural plasticity and the
mechanisms whereby long-term memory is stored (Huang
1995; Lisman et al., 2011; Morikawa and Paladini, 2011).
There is evidence that the D1 dopamine receptor is involved
in ORM consolidation. De Lima et al. (2011) showed that sys-
temic injections of the D1 receptor agonist SKF38393 at
5 mg/kg produce an enhancement of object recognition mem-
ory when tested 24 and 72 h after the sample phase. Con-
versely, systemic injections of the D2 dopamine receptor
agonist quinpirole at two doses (1 mg/kg and 5 mg/kg) did not
affect memory. It is noteworthy that other studies have shown
that D1/D5 (but not D2) receptor activity are involved in plas-
tic events (late phase LTP) related to memory consolidation,
suggesting that D1/D5 receptor activity may be involved in the
late phase of protein synthesis-dependent component of LTP
(Huang and Kandel, 1995).
Studies with systemic injections give us a first and important
approach to the role of the D1 receptor in object recognition
memory consolidation (Hotte et al., 2005; de Lima et al.,
2011); our study gives an extended idea of which structures are
involved in consolidation through D1 dopamine receptor activ-
ity. We found that the PRH and the HIP have a differential
participation in consolidation of object familiarity. Our results
indicate that the activity of these receptors in the PRH is nec-
essary for object recognition memory consolidation while the
activity in the HIP is not. Moreover, the D1 receptor agonist
SKF38393 infused in the PRH enhances the consolidation in a
protocol in which a short sample phase is not enough to
 D1 RECEPTOR MODULATES RECOGNITION MEMORY CONSOLIDATION
generate long-term memories in control animals. The enhance-
ment of memory is consistent with the idea that changes in
synaptic strength underlying memory could be promoted by
dopamine (Huang 1995; Bethus et al., 2010; Lisman et al.,
2011; Morikawa and Paladini, 2011).
It is commonly accepted that recognition memory has at
least two components: the judgment of familiarity of stimuli
and the recollection of contextual information where stimuli
are experienced (Brown and Aggleton, 2001; Yonelinas et al.,
2002). A large body of literature suggests that PRH and HIP
contribute differentially to these components. For example: sev-
eral studies suggest that the PRH is necessary for consolidation
of information about objects (Winters and Bussey, 2005; Bal-
deras et al., 2008), while the HIP is necessary for consolidating
contextual information where objects were experienced (Balde-
ras et al., 2008; Hardt et al., 2010; Barker and Warburton,
2011). Our results support the notion that information about
single stimulus is processed in the PRH. Further studies will be
designed to reveal the mechanisms by which D1 facilitates rec-
ognition memory consolidation in the PRH.
Detailed Methods
Adult male Wistar were used rats from our Institute breed-
ing colony, (300 g) at the beginning of the experiments. Rats
were implanted bilaterally with guide cannulae at the PRH,
posterior 3, lateral 6 6.5, ventral 7, or the dorsal HIP; poste-
rior 3.6, lateral 6 3.0, ventral 3.3. [Coordinates of the infusion
sites from bregma (mm) (Paxinos and Watson, 1998)]. Histol-
ogy analysis revealed that animals included in the study had
the needle tips in the cerebral region of interest [PRH: 23.14
to 23.60; HIP: 23.60 to 23.80 mm with respect to Bregma.
For a detailed method in histology analysis please see (Balderas
et al., 2012).
The D1 dopamine receptor antagonist R (1)-SCH-23390
hydrochloride (SCH23390) (Sigma, St Louis, MO) was used.
The dose (2 mg per side) was based on previous studies that
reported impaired memory consolidation (Guzman-Ramos
et al., 2010). We used the D1 dopamine receptor agonist
(6)-SKF-38393 hydrochloride (SKF38393) (Sigma, St Louis,
MO) at a dose of 12.5 mg per side, based on previous studies
that show that this dose is effective in enhancing memory con-
solidation (Rossato et al., 2009; Fiorenza et al., 2012).
The groups tested for STM with D1 antagonist infusions
were: PRH-VEH (n 5 7), PRH-SCH23390 (n 5 9), HIP-VEH
(n 5 8), HIP-SCH23390 (n 5 7). For LTM: PRH-VEH
(n 5 15), PRH-SCH23390 (n 5 15), HIP-VEH (n 5 8), HIP-
SCH23390 (n 5 8). The groups tested for STM with D1 agonist
infusions were: PRH-VEH (n 5 9), PRH-SKF38393 (n 5 8),
HIP-VEH (n 5 6), HIP-SKF38393 (n 5 7). The groups used
for LTM were: PRH-VEH (n 5 9), PRH-SKF38393 (n 5 10),
HIP-VEH (n 5 7), HIP-SKF38393 (n 5 7). All experiments
were carried out in independent groups.
The general protocol used for animal manipulation and
object recognition memory task has been described in detail
877
elsewhere [see (Balderas et al., 2012)]. In this study we used
two durations for the sample phase (3 and 5 min).
ACKNOWLEDGMENTS
The authors acknowledge O. Carbajal for technical support,
Jean-Pascal Morin for his text review and M. Santoyo, A. Daz,
D. Ortega, and K. Uribe for their assistance with the
experiments.
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