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Neurobiology of Learning and Memory 96 (2011) 272279

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Neurobiology of Learning and Memory


journal homepage: www.elsevier.com/locate/ynlme

Contribution of the parafascicular nucleus in the spontaneous object


recognition task
Edwin Castiblanco-Pieros, Maria Fernanda Quiroz-Padilla ,
Carlos Andres Cardenas-Palacio, Fernando P. Cardenas
Laboratorio de Bases Biolgicas del Comportamiento, Facultad de Psicologa, Universidad de la Sabana, Bogot, Colombia
Laboratorio de Neurociencias y Comportamiento, Departamento Psicologa, Universidad de los Andes, Bogot, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: The parafascicular (PF) nucleus, a posterior component of the intralaminar nuclei of the thalamus, is con-
Received 24 February 2011 sidered to be an essential structure in the feedback systems of basal gangliathalamo-cortical circuits
Revised 11 May 2011 critically involved in cognitive processes. The specic role played by multimodal information encoded
Accepted 13 May 2011
in PF neurons in learning and memory processes is still unclear. We conducted two experiments to inves-
Available online 23 May 2011
tigate the role of the PF in the spontaneous object recognition (SOR) task. The behavioral effects of pre-
training rats with bilateral lesions of PF with N-methyl-D-aspartate (NMDA) were compared to vehicle
Keywords:
controls. In the rst experiment, rats were tested on their ability to remember the association immedi-
Intralaminar thalamic nuclei
NMDA lesions
ately after training trials and in the second experiment after a 24 h delay. Our ndings provide evidence
Spontaneous object recognition task that PF lesions critically affect both SOR tests and support its role in that non-spatial form of relational
Prefrontal cortex memory.
Relational memory 2011 Elsevier Inc. All rights reserved.

1. Introduction Single-axon tracing studies have indicated that virtually all PF


neurons project to both cerebral cortex and striatum (Deschenes,
The parafascicular nucleus (PF) in rats and the centromedian Bourassa, Doan, & Parent, 1996). Anatomically, the PF is a major
parafascicular complex (CMPF) in primates and other mammals source of excitatory projections to striatum and prefrontal cortices
are the so-called posterior intralaminar nuclei (pIL) of the thalamus. (PFC), mainly prelimbic, and less abundantly to cingulate regions
These nuclei are a critical component of the ascending reticular acti- (Berendse & Groenewegen, 1991; Deschenes et al., 1996; Marini,
vating system (ARAS) and the basal gangliathalamocortical circuit Pianca, & Tredici, 1996; Parent & Parent, 2005; Smith, Raju, Pare,
(Groenewegen & Berendse, 1994; Parent & Parent, 2005; Van der & Sidibe, 2004; Vercelli, Marini, & Tredici, 2003). In relation to stri-
Werf, Witter, & Groenewegen, 2002). In general, damage to intra- atum projections, the lateral PF projects to the putamen, the lateral
laminar nuclei has been associated with signs of amnesia (Bailey & globus pallidus and more diffusely to dorsolateral caudate, areas
Mair, 2005; Mitchell & Dalrymple-Alford, 2005; Newman & Burk, that are related to sensory-motor function. The medial PF projects
2005; Quiroz-Padilla, Marti-Nicolovius, & Guillazo-Blanch, 2010; to the ventral pallidus and in lesser amounts to the accumbens and
Savage, Castillo, & Langlais, 1998; Van der Werf, Jolles, Witter, & Uy- olfactory tubercle, regions both related to associative-limbic func-
lings, 2003), and functions as arousal (Mancia & Marini, 1995; tions (Otake & Nakamura, 1998; Smith et al., 2004; Van der Werf
Marini, Tredici, & Mancia, 1998; Shirvalkar, Seth, Schiff, & Herrera, et al., 2002). The cognitive decits observed after PF lesions are
2006; Steriade & Deschenes, 1984; Van der Werf et al. 2002), atten- thought to arise from the combined deafferentation of PFC and stri-
tion (Bailey & Mair, 2005; Burk & Mair, 2001; Kinomura, Larsson, atum targets (Van der Werf et al., 2003). The effect of PF manipu-
Gulyas, & Roland, 1996; Minamimoto & Kimura, 2002; Newman & lations on memory functions should be specically related to the
Burk, 2005; Newman & Mair, 2007) and pain (Cheng et al., 2009; neural systems innerved. The PF has a strategic location to be con-
Dupouy & Zajac, 1997; Gao et al., 2010; Liu, Qiao, & Dafny, 1993; sidered an excellent candidate for investigating memory processes.
Vogt, Hof, Friedman, Sikes, & Vogt, 2008), in humans and other However, before concluding PF participation in non-spatial rela-
animals. tional memory it is necessary to rule out any possible decits in
locomotion induced by the excitotoxic lesion. So an open eld loco-
motion assessment was carried out before the spontaneous object
Corresponding author. Address: Facultad de Psicologa, Universidad de la
recognition (SOR).
Sabana. Campus Universitario del Puente del Comn, Autopista Norte de Bogot,
The link between PF and cognitive processes has traditionally
DC, Colombia. Fax: +57 861 2721.
E-mail address: mariaqp@unisabana.edu.co (M.F. Quiroz-Padilla). been investigated through rat studies of radiofrequency (Nyakas,

1074-7427/$ - see front matter 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.nlm.2011.05.004
E. Castiblanco-Pieros et al. / Neurobiology of Learning and Memory 96 (2011) 272279 273

Veldhuis, & De Wied, 1985; v Wimerdma Greidanus, Bohus, & de (60  60  40 cm high) with the oor covered with an acrylic
Wied, 1974) or electrolytic (Cardo & Valade, 1965; Guillazo- surface. The objects were made of plastic, aluminum or glass with
Blanch et al., 1995; Massanes-Rotger, Aldavert-Vera, Segura- differences in color, height (between 8 and 15 cm), weight (between
Torres, Marti-Nicolovius, & Morgado-Bernal, 1998; Redolar-Ripoll 55 and 226 g), shape and texture (Fig. 1). After each session, the
et al., 2003; Shapovalova, Pominova, & Dyubkacheva, 1997; objects and surface of the open box were cleaned with acetic acid
Thompson, Kao, & Yang, 1981; Tikhonravov, 2000) lesions. There (10%) to avoid olfactory cues.
are only three studies (MHarzi, Jarrard, Willig, Palacios &
Delacour, 1991; Quiroz-Padilla, Guillazo-Blanch, Vale-Martinez, & 2.1.2. Analysis of behavior
Marti-Nicolovius, 2006; Quiroz-Padilla, Guillazo-Blanch, Vale- The animals were videotaped while performing both the
Martinez, Torras-Garcia, & Marti-Nicolovius, 2007) evaluating the locomotion tests and the SOR task. Object exploration was opera-
effects of excitotoxic lesions restricted to PF area in four different tionally dened as physical contact with the object through
memory tasks: two of procedural memory (the appetitively moti- forepaws or snout. Distances >2 cm, as well as sitting or standing
vated odor discrimination and the aversively motivated two-way ac- on the object with the nose facing the ceiling were not considered
tive avoidance tasks) (Quiroz-Padilla et al., 2007), and two of exploratory behavior. For the SOR task training the dependent
relational memory (the object recognition and the social transmis- variables were: the mean time spent exploring the objects and
sion of food preference (MHarzi et al., 1991; Quiroz-Padilla et al., the mean average frequency of contact with the objects. For the
2006). The lack of knowledge of the specic participation of PF in SOR task test, a discrimination ratio was used (discrimination
memory processes urges the need to continue researching on its role ratio = novel object exploration/total interaction with all the
in cognitive function. objects) (see Bevins & Besheer, 2006).
The main purpose of the present study is to identify the contri- The frequency of following behaviors were analyzed in the loco-
bution of the PF nuclei to non-spatial relational memory by using motion tests: crossing the lines that divided the cylindrical open
the SOR task. Ennaceur and Delacour (1988) proposed differential eld bearing in mind that the animals hind paws crossed the line
patterns of exploration for familiar and novel objects maybe as a between each quadrant; standing on their hind paws in the eld
result of the natural tendency to explore novel objects. An impor- (rearing); licking or scratching themselves (grooming); elongation
tant advantage of SOR is that no aversive/stressful stimuli are of the head and shoulders followed by retraction to its original
needed. Other feature of the task is the requirement of perirhinal position (stretching); and remaining stationary showing piloerec-
(PRh) cortex integrity to discriminate novel objects (Aggleton, tion (freezing). Each of these behaviors was measured before and
Albasser, Aggleton, Poirier, & Pearce, 2010; Brown & Aggleton, after of the surgery, and a delta score was obtained; this delta score
2001; Clark & Squire 2010; Murray & Bussey, 1999; Winters, is dened as: frequency of the behavior before surgery - frequency
Saksida, & Bussey, 2008). Previous studies (Bussey, Duck, Muir, of the behavior after surgery. These dates were collected with the
and Aggleton, 2000; Ennaceur, Neave, & Aggleton, 1996) reported software X-Plo-Rat 2005 1.1. (Taverna-Chaim & Morato, 2008).
impaired object recognition memory in the SOR task following
neurotoxic PRh damage in rat. The PRh cortex is responsible for 2.1.3. Measurements and statistical analysis
familiarity discrimination however, this kind of memory involves All statistical analyses were carried out by using SPSS for
interaction with other structures outside the medial temporal lobe Windows, version 17.0. The comparison of the averages of the
as PFC. According to this idea we can speculate that PF lesions groups for all SOR task measures was done using Student t test
decreased the cortical activation required to discriminate signi- for independent samples. In order to compare the results in loco-
cant events in the SOR task, therefore memory can be affected. This motion tests, a Student t test for independent samples was done
could presumably be a result of PF deafferentation of important using delta scores for each behavior (crossing, rearing, grooming
system components of basal gangliathalamic-cortex circuit, par- and stretching). Other analyses were carried out to assess the effect
ticularly PFC (Berendse & Groenewegen, 1991; Deschenes et al., of bilateral PF lesions on object exploratory behaviors and there-
1996; Heidbreder & Groenewegen, 2003; Hsu & Price, 2007; fore discard any effect of lesion on the SOR task. In this regard,
Macchi & Bentivoglio, 1986; Marini et al., 1996; Otake & General Lineal Model for repeated measures was used with corre-
Nakamura, 1998; Parent & Parent, 2005; Sadikot & Rymar, 2009; sponding contrasts (simple for between-groups effects and polyno-
Smith et al., 2004; Van der Werf et al., 2002; Vercelli et al., 2003; mial and repeated for within-group effects), in which the
Vertes, 2004). independent variables were Group (Lesion and Vehicle) and the
The nding of impairments in two different retention delays:
immediately and/or 24 h after training, in rats submitted to bilat-
eral lesion with N-methyl-D-aspartate (NMDA) should support
the contribution of PF in the memory process of the SOR task.

2. Materials and methods

2.1. General methods: Experiments 1 and 2

Both experiments were performed taking into account the


ethical and legal standards required for laboratory animal research
in Colombia (Estatuto Nacional de Proteccin Animal Law 84 of
1989 and Resolution Number 008430 of 1993 of the Ministerio de
la Salud).

2.1.1. Apparatus
A cylindrical open eld (55  60 cm; diameter and height) was
used to assess locomotion before and 6 days after surgery. The SOR
task was carried out in an open box made of wood Fig. 1. Photograph of the objects used in the spontaneous recognition task.
274 E. Castiblanco-Pieros et al. / Neurobiology of Learning and Memory 96 (2011) 272279

dependent variables were: approaches 62 cm, contact with fore- described) without objects. Then, three 5-min training trials were
paws, and snout. In the statistical procedures used in this study done, with inter-trial intervals of 2 min. In each trial, the animals
an alpha of p 6 0.05 were assumed, with a reliability of 95%. were placed in the corner of the open eld where there was not
object, looking at the vertex of the walls. All other three corners
2.2. Experiment 1 had a different object. These three objects were the same in all
three trials for each subject, but among trials the objects were
2.2.1. Subjects rotated taking care of do not to repeat the location, to reduce place
Twenty-four male Wistar rats obtained from Inmunopharmos preferences. The test session took place two minutes after comple-
laboratories were used in the experiment. At the beginning of the tion of training trials and lasted ve minutes. In this session, one of
study the mean age of the animals was 98 days (SE = 3.87) and the three objects previously used (familiar objects) was replaced
mean weight of 291.48 g (SE = 8.09). Throughout the period of by a new object with which the animal had never had contact.
the experiment the animals were housed individually in plastic-
bottomed cages (48  38  20 cm) with sawdust bedding. During 2.2.4. Histology
all stages of the investigation the animals were kept under con- After the behavioral procedures, all animals were deeply anes-
trolled temperature settings (2024 C), humidity (4070%) and a thetized with an overdose of sodium pentobarbital (Euthanex,
12 h lightdark cycle (lights on at 8:00 a.m.). All experimental pro- Invet s.a., 200 mg/kg) and were perfused transcardially with 0.9%
cedures were performed during articial light cycle. During the saline followed by 10% formalin-saline. Brains were extracted
experiment the animals were supplied with food and water ad libi- and post-xed in formalin for at least 24 h and then submerged
tum, and their weight and cleanliness were monitored. in a 30% sucrose solution prior to sectioning. Coronal 40-lm
sections were cut out on a cryostat (Leica Microsystems, model
2.2.2. Surgical procedure CM1850), mounted and stained with Cresyl violet. The sections
Before surgical procedure, the animals were randomly assigned were examined under a light microscope (Nikon Eclipse 80i)
to Lesion or Vehicle groups. Rats were anaesthetized with and microphotographs were taken with a digital camera (Nikon
intraperitoneal injection of ketamine hydrochloride (ketamine Ds-Fi1). The tissue evaluation was done using a blind strategy:
50, Holliday-Scott SA, 75 mg/kg) and xylazine (Seton, Calier; two observers who were not aware of the behavioral results inde-
10 mg/kg), and placed in a stereotaxic instrument (Stoelting Co., pendently examined the brain sections. The lesions were recon-
Model 51725) with the incisor bar set 3.3 mm below the interaural structed on standardized sections of the rat brain (Paxinos &
line. Before the skin incisions, local anesthesia was administered Watson, 1997).
by subcutaneous application of lidocaine (Roxicaina 1%, Ropsohn
Therapeutics Ltda). The skull was exposed through a midline inci- 2.3. Experiment 2
sion and leveled along the bregma-lambda axis. Two holes were
drilled in the cranium of the animals and a 26-gauge needle Ham- 2.3.1. Subjects
ilton syringe was lowered to the targets according to the following Twenty-four male Wistar rats obtained from Inmunopharmos
stereotaxic coordinates (Paxinos & Watson, 1997): anteroposterior laboratories were used in the experiment. At the beginning of the
(AP) 4.1 mm from bregma, lateral (L) 0.6 mm from midline, and study the mean age of the animals was 100 days (SE = 4.7) and
dorsoventral (DV) 6.1 mm and 5.6 mm from the skull surface. mean weight of 295,98 g (SE = 12.16). During all stages of the
Before the infusion, the needle was left in place for 30 s. Animals study, the animals were handled with the same parameters for
belonging to the lesion group were infused bilaterally at the PF nu- maintenance and control described in Experiment 1.
cleus the excitotoxin NMDA (SigmaAldrich, 0.15 M in sterile
phosphate-buffered, saline, pH 7.4). A digital microinjector (Stoel-
2.3.2. Surgical procedure
ting Quintessential Injector, model 5331) was used for all
Before surgical procedure, rats were randomly assigned to
infusions. The total volume of infusion for each hemisphere was
LESION or VEHICLE groups. The surgical protocol was the same
1.2 ll. At the rst depth 0.8 at a rate of 0.133 ll per minute were
as in Experiment 1,
infused. While 0.4 at a rate of 0.1 ll per minute were infused at
the second depth. The rst infusion was made in the DV deeper
2.3.3. Behavioral tasks
coordinate (DV 0.61 mm). The needle was allowed to sit for
The experimental conditions were similar to those used in
10 min before being raised to avoid the spread of NMDA up the
Experiment 1, except that the test session took place 24 h after
needle tract. The scalp was then sutured and a topical antiseptic
completion of training trials.
was administered to prevent infections (Isodine, Boehringer
Ingelheim S.A.). Throughout the procedure, the animals body
temperature was kept constant with a thermal blanket. Vehicle 2.3.4. Histology
rats underwent the same procedure, except that sterile phos- The histological procedures and the criteria applied were the
phate-buffered saline was infused. same as in Experiment 1.

2.2.3. Behavioral tasks 3. Results


In the rst phase of the experiment, each rat was kept in indi-
vidual plastic cages. In order to animals get familiarized to the 3.1. Histology
investigator, all rats were handled for 5-min each day for a period
of 4 days. On the fth day the locomotion pre surgery test was Fig. 2A and B shows the maximum and minimum extents of
done by placing the animals in the cylindrical open eld for successful PF lesions for each plate (gures modied from Paxinos
5 min. Then the rats had 2 days without treatment before the sur- & Watson, 1997). Final sample included only rats with bilateral
gery. All animals were allowed to recover for 7 days previous to lesions P40% in the PF, damage that extended from 3.80 mm to
locomotion post surgery test, which was performed for 5 min in 4.52 mm posterior to bregma (Paxinos & Watson, 1997). The
the same cylindrical open eld used in the pre surgery tests. Next lesions were characterized by loss of neurons, glyosis and traces
day, the SOR task was applied to the animals. First, each rat had a of necrosis adjacent to the tracks made by the needle (Fig. 3A
habituation session for ve minutes in the open eld (above D). The axons in the fasciculus retroexus remained visible in all
E. Castiblanco-Pieros et al. / Neurobiology of Learning and Memory 96 (2011) 272279 275

Fig. 2. Schematic drawing of the smallest (gray area) and the largest (striped area) PF lesions in successive anterior/posterior coronal sections in Experiment 1 (A) and
Experiment 2 (B). The extent of the lesions is superimposed on gures modied from Paxinos and Watson (1997).

subjects included in the nal sample. For both experiments, histo- < 0.05]. This nding suggests that lesions in PF change the normal
logical analyses were performed by two independent blind functioning of object recognition memory when performing the
observers. test 2 min. after training. There were no signicant differences be-
tween groups in the total time exploring objects during the trial
3.2. Behavior sessions [t(16) = 1983; p = 0065], in the total frequency of contact
with objects in the trial sessions [t(16) = 0587; p = 0566] and in
3.2.1. Experiment 1 the total time exploring objects during the test session
The nal sample was made up of 18 rats distributed into LESION [t(16) = 1277; p = 0220] (Fig. 4 B). General lineal model for re-
(n = 8) and VEHICLE (n = 10) groups. peated measures showed no signicant differences in the explora-
tion time [F(1,16) = 3935, P = 0.65], as well as the frequencies of
3.2.1.1. Locomotion test. In order to assess any possible effect of sur- approaches 62 cm [F(1,16) = 0136, P = 0, 717], and contacts with
gery upon locomotion and motility, Student t tests were conducted forepaws [F(1,16) = 2947, P = 0, 105], and the snout [F(1,16) = 0330,
on delta scores (differences between data at the pre and post surgery P = 0, 574].
sessions) (see page 8 for description) for crossings, grooming, rear-
ing, stretching and freezing. Independent samples t-test analysis
3.2.2. Experiment 2
showed that there were not differences between the groups in delta
The nal sample was made up of 17 rats distributed into LESION
scores for crossings [t(16) = 0563; p = 0581], rearing [t(16) = 0.07;
(n = 7) and VEHICLE (n = 10) groups.
p = 0945], grooming [t(16) = 0989; p = 0337] and stretching
[t(16) = 0243; p = 0811]. None of the subjects regardless of the group
showed immobility or piloerection (freezing). These results indicate 3.2.2.1. Locomotion test. Independent samples t-test analysis
that lesions did not affect the locomotor activity of animals. showed that there were not differences between the groups in delta
scores for crossings [t(15) = 0245; p = 0810], rearing [t(15) = 0095;
3.2.1.2. Spontaneous object recognition task. Fig. 4A shows the p = 0926], grooming [t(15) = 0373; p = 0715] and stretching
discrimination ratio of the novel object for all the groups in the [t(15) = 0967; p = 0349]. None of the subjects regardless of the
test. Student t-test showed signicant differences between the group showed immobility or piloerection (freezing). The ndings
groups in the discrimination ratio [t(16) = 2162; p = 0.0461 are consistent with those found in Experiment 1, conrming that
276 E. Castiblanco-Pieros et al. / Neurobiology of Learning and Memory 96 (2011) 272279

Fig. 3. Photomicrographs of Cresyl violet-stained coronal sections (40 lm thick), about 4.30 mm posterior to bregma, showing the appearance of a typical NMDA bilateral PF
lesion (A) and (B) compared to a vehicle-infused subject (C) and (D). Scale bar = 1.00 mm in (A), (B), (C) and (D). PF, parafascicular; fr, fasciculus retroexus.

Fig. 4. Experiment 1, (A) Discrimination ratio of the novel object two minutes after training trials for both groups. (B) Differences between groups in the total time exploring
objects during the trial sessions (P < 0.05).

the PF nucleus lesions did not affect the locomotor activity of the To complement the analysis of exploratory behavior, general
experimental subjects. lineal model for repeated measures was conducted for the trial ses-
sions. There were no signicant differences between groups
3.2.2.2. Spontaneous object recognition task. Analysis of the discrim- [F(1,15) = 0057, P = 0815]. This result supports the evidence that
ination ratio revealed that there are signicant differences the PF nucleus lesion did not affect exploratory behavior. In the
between the control group and lesion group [t(15) = 4890; analysis of object exploration during the trial phases there were
p < 0.001] (Fig. 5 A). This result suggests that lesions in PF produce no differences groups for the frequency of approaches 6 2 cm
a decit in object recognition memory at 24 h. Moreover, There [F(1,15) = 0031, P = 0863], the frequency of contacts with snout
were no signicant differences between groups in the total time [F(1,15) = 0.41, P = 0842], and with forepaws [F(1,15) = 1282,
exploring objects during the trial sessions [t(15) = 0238; P = 0275]. These results, together with those obtained in Experi-
p = 0815], in the total frequency of contact with objects in the trial ment 1, suggest that bilateral lesions of the PF nucleus did not
sessions [t(15) = 0.091; p = 0929] and in the total time exploring affect object exploration and, therefore, did not inuence animal
objects during the test session [t(15) = 1707; p = 0108] (Fig. 5 B). performance in SOR task.
E. Castiblanco-Pieros et al. / Neurobiology of Learning and Memory 96 (2011) 272279 277

Fig. 5. Experiment 2, (A) Discrimination ratio of the novel object 24 h after training trials for both groups. (B) Differences between groups in the total time exploring objects
during the trial sessions (P < 0.001).

4. Discussion nucleus, in different animal models used to evaluate this kind of


memory (Burk & Mair, 1999; Langlais & Savage, 1995; Porter, Koch,
The present study evaluated the effects of bilateral NMDA & Mair, 2001; Savage et al., 1998). Furthermore, Smith, Country-
lesions of the PF nucleus on a SOR task. In this paradigm, rats were man, Sahuque, and Colombo (2007) found that the acquisition
required to remember familiar objects immediately or 24 h after. and remembering in the socially transmitted food preference task
The main results showed that PF lesions impair SOR at both reten- (model of non-spatial relational memory) induces activation of the
tion delays. These ndings suggest that PF is involved in the object medial prefrontal cortices (PFCm), specically in the prelimbic and
recognition memory. infralimbic cortex.
Regarding to exploration or motor behavior in both experi- Concerning to object recognition memory, there are studies
ments, there were no signicant differences between groups in showing connection between this kind of memory and PFCm
crossing, rearing and stretching frequency in the open eld. There cortex, especially with the prelimbic area (Barker, Bird, Alexander,
were no signicant differences between groups in both frequency & Warburton, 2007; Christoffersen et al., 2008; DeVito &
or time spent exploring the sample objects in the SOR task or in Eichenbaum, 2010; Levallet, Hotte, Boulouard, & Dauphin, 2009).
other exploratory behaviors (approaches 6 2 cm, contact with fore- Barker et al. (2007), suggest that object recognition memory in rats
paws and snout). No signicant changes were observed in the over- requires judgments on the previous occurrence of stimuli made on
all exploration time in the test session. the basis of the relative familiarity with each object. It has been
Altogether, these ndings dismiss the incidence of variables proposed that PFCm may be related to the discrimination required
other than memory and maybe learning on the performance of le- for object recognition test in order to establish an order or timing
sioned animals in the SOR task. The explanations for the results ob- of the objects presentation (Dere, Huston, & De Souza Silva, 2007).
tained in this investigation are based on the fact that the PF Our results contrast with those reported by MHarzi, et al.
nucleus participates in the ARAS, as well as in the basal ganglia (1991), who found no impairment on object recognition memory
thalamic-cortex circuit; both systems related to generalized activa- after ibotenic acid lesion of PF in rats. This divergence in results
tion or arousal (Jones, 2003; Quiroz-Padilla et al., 2010), attention may be due to some methodological differences such as the kind
(Heidbreder & Groenewegen, 2003; Hulme, Whiteley, & Shipp, of the object recognition task used. In the experiments reported
2010; Matsumoto, Minamimoto, Graybiel, & Kimura, 2001; Mina- here, three trials before the test session were done using three ob-
mimoto, Hori, & Kimura, 2005; Minamimoto & Kimura, 2002; Rae- jects per session, whereas in the study of MHarzi et al. (1991),
va, 2006; Smith et al., 2004), learning and memory (Guillazo- there was only one trial before test and two objects per session.
Blanch et al., 1995; Massanes-Rotger et al., 1998; Quiroz-Padilla Our variation increases the difculty of the SOR task, demanding
et al., 2006; Quiroz-Padilla et al., 2007). so a greater degree of arousal and attention in order to properly ac-
According to this evidence it is hypothesized that the PF lesions quire and store it. Moreover, this study adds to emerging evidence
decreased the cortical activation required to discriminate signi- of the involvement of PF non-spatial relational memory, as was
cant events in the SOR task, therefore memory can be affected. This suggested in the study reported by Quiroz-Padilla et al. (2006),
could presumably be a result of PF deafferentation of important and complements the work involving PF with other kinds of rela-
system components of basal gangliathalamic-cortex circuit, par- tional memory (Bailey & Mair, 2005; Burk & Mair, 1998; Lopez
ticularly PFC (Berendse & Groenewegen, 1991; Deschenes et al., et al., 2009; Porter et al., 2001; Savage, Sweet, Castillo, & Langlais,
1996; Heidbreder & Groenewegen, 2003; Hsu & Price, 2007; Mac- 1997; Savage et al., 1998; Van der Werf et al., 2003).
chi & Bentivoglio, 1986; Marini et al., 1996; Otake & Nakamura, Given that an optimal level of alertness is required for learning
1998; Parent & Parent, 2005; Sadikot & Rymar, 2009; Smith and behavior to occur, and that the PFCm is critically involved in
et al., 2004; Van der Werf et al., 2002; Vercelli et al., 2003; Vertes, alertness (Robbins & Everitt, 1995; Valds & Torrealba, 2006), it is
2004). possible that the decit observed in object recognition test could
There are some reports on memory impairment after lesions in be the result of alterations in glutamatergic neurons projecting from
the intralaminar nuclei, including the PF nucleus, very similar to PF to PFCm, particularly to prelimbic cortex region directly related
those caused by hypofunction of PFC (Burk & Mair, 1998; Van to ARAS and relational memory processes. The deafferentation of the
der Werf et al., 2003). Indeed, there have been reported decits prelimbic cortex could have decreased the cortical activation re-
in working memory after thalamic damage, including the PF quired for encoding information and memory formation. This idea
278 E. Castiblanco-Pieros et al. / Neurobiology of Learning and Memory 96 (2011) 272279

is consistent with the ndings reported by DeCoteau, McElvaine, Bailey, K. R., & Mair, R. G. (2005). Lesions of specic and nonspecic thalamic nuclei
affect prefrontal cortex-dependent aspects of spatial working memory.
Smolentzov, and Kesner (2009), according to which the animals with
Behavioral Neuroscience, 119(2), 410419.
prelimbic/infralimbic cortex lesions displayed a profound and sus- Barker, G. R., Bird, F., Alexander, V., & Warburton, E. C. (2007). Recognition memory
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