Brain Research Bulletin 79 (2009) 436440

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Brain Research Bulletin

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

Research report

What are the functions of sh brain pallium?

Juan Pedro Vargas , Juan Carlos Lpez, Manuel Portavella
Laboratorio de Neurociencia de la Conducta (LNC), Departamento de Psicologa Experimental, Facultad de Psicologa,
Universidad de Sevilla, C/Camilo Jos Cela s/n, E-41018, Sevilla, Spain

a r t i c l e

i n f o

Article history:
Received 13 February 2009
Received in revised form 6 May 2009
Accepted 11 May 2009
Available online 20 May 2009
Keywords:
Amygdala
Hippocampus
Isocortex
Brain evolution
Goldsh

a b s t r a c t
There is some experimental evidence that the pallial areas of a shs brain are involved in distincted
learning functions. Recently published data suggest that the medial pallium is essential for avoidance
learning and the lateral pallium is crucial for spatial learning and is also involved in temporal aspects
of the learning processes. This data joined to the proposal of homologies between medial and lateral
sh pallia and pallial amygdala and hippocampus respectively, suggest that the pallial areas could have
preserved their functions throughout vertebrates evolution. However, the functional implication of dorsal
pallium that has been proposed as homologous to mammalian isocortex and transition cortex is largely
unknown. In this study we analyze the role of dorsal pallium in trace and non-trace avoidance learning.
Our results show the implication of this area in trace conditioning, but not in non-trace conditioning. This
result allows discussion of homology proposals among lateral, dorsal, and medial pallia and hippocampus,
isocortex, and pallial amygdala respectively.
2009 Elsevier Inc. All rights reserved.

1. Introduction
Experimental evidence from neurobehavioral studies suggest
that the lateral pallium (LP) and the medial pallium (MP) of the
sh brain might have similar involvements in learning as their
homologous structures, hippocampus and the amygdala respectively [10,3032]. Thus, the MP is essential for emotional learning
and related processes (i.e. avoidance learning: [3032]), while
the LP is crucial for spatial learning based on landmark sets
[10,32,35]. Recent ndings show that lesions to the MP impair
both the acquisition and the retention of a conditioned avoidance response under massive and spaced-trial training, both in
trace and non-trace procedures [3032]. Also, a lesion to the LP
impairs the retention of avoidance response only in trace conditioning tasks [30,31]. This set of data has produced an initial
interpretation of sh pallial functions: the ventral MP is involved
in emotional learning as is the pallial amygdala [1,6,14], and the
ventral LP is involved in spatial and/or relational, and temporal characteristics of learning [7,8,13,18,27,28,34] as is the hippocampus
[10,3032]. In addition, there is another structure of the telencephalic pallium of sh that has not been an object of study
until now. This pallial region known as DP, the dorsal pallium,
has been proposed as homologous to mammalian isocortex and
transition cortex [4,24,25]. In fact, according to Nieuwenhuys and
Meek [20] nomenclature, the named regions of DP, dorsodorsal

Corresponding author. Tel.: +34 954 55 4401; fax: +34 954 55 1695.
E-mail address: vargas@us.es (J.P. Vargas).
0361-9230/$ see front matter 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.brainresbull.2009.05.008

telencephalon (Dd), dorsomedial pars dorsalis telencephali (Dmd),

and dorsolateral pars dorsalis telencephali (Dld) present a similar
pattern of connectivity which is different from the medial ventral part of the MP (dorsomedial pars ventralis telencephali, Dmv),
proposed as homologous to the pallial amygdala [3,5,20,21,23]
and to the ventral part of the LP (dorsolateral pars ventralis
telencephali, Dlv), proposed as homologous to the hippocampus
[3,5,20,21,23].
The analysis of the dorsal pallium structure is interesting due
to the underlying learning processes. An isocortex-like structure
could control short-term memory processes and play an important
role in the performance of activity under timing implications. To
explore the functional activity of this neural structure, the present
study analyzes the implication of the DP in avoidance learning in
trace and non-trace procedures and explores the specic function
of major areas of sh brain pallium.
2. Material and methods
2.1. Experiment 1: Non-trace two-way active avoidance
conditioning
Fifteen experimentally naive goldsh (Carassius auratus),
obtained from a local supplier, served as subjects. The sh measured between 8 and 11 cm in length, were kept in a 200 L glass
aquarium with aerated and ltered water, and kept at a constant
temperature of 20 C. The room was on a constant 14/10 h light/dark
cycle. Pellets of dry food were provided daily ad libitum during
the experimental period. Use and handling of the subjects were

J.P. Vargas et al. / Brain Research Bulletin 79 (2009) 436440

in accordance with Directive 86/609/CEE of the European Community Council and Spanish Real Decreto 223/1988. The apparatus
and experimental procedures have been extensively described in
a previous article [30]. Briey, four similar water-lled shuttle
boxes (50 25 14 cm) were used. The shuttle boxes allowed the
presentation of a green light (10 W, 220 V AC, 50 Hz) used as a discriminative stimulus and a mild electric shock (0.39 V/cm, 50 Hz,
pulsed 200 ms on and 800 ms off) used as an aversive stimulus.
The shuttle boxes were divided into two compartments by means
of a trapezoidal barrier. Two pairs of photoreceptors and photoemitters placed on the barrier allowed to detect the subjects
responses. A computerized system (Letica SL) and software (Skinner; Cibertec SA) recorded sh responses stimulis delivery. Fish
were pre-exposed individually to the shuttle-boxes for three consecutive days (see [31], for details).The procedure consisted of daily
sessions of 10 trails each separated by an inter-trial interval (ITI) of
varying duration (between 1 and 2 min). The temporal separation
between discriminative stimulus onset and aversive onset was 10 s
(assuming a negative response). If the sh responded, by swimming across the barrier, within the rst 10 s its response canceled
the discriminative stimulus presentation and the aversive stimulus
was not administered. However if the subject did not respond to
the discriminative stimulus within the rst 10 s of green light onset,
the aversive stimulus was turned on until the subject produced the
proper response or for a maximum of 5 s, whichever came rst, at
which point both stimuli were turned off simultaneously. Learning
criterion of at least 70% of avoidance responses was established in
ve out of six consecutive training sessions. All subjects reached the
criterion between sessions 6 and 15 and were randomly assigned
to one of three groups: dorsal pallium (DP) ablation (n = 7), shamoperated (n = 4), and intact (n = 4). The variables recorded for the
criterion sessions were percentage of avoidance (shuttle responses
occurring before shock onset; the latency was <10 s) and percentage
of escape (shuttle responses occurring during the shock; the latency
was between 10 and 15 s). ANOVA with repeated measurements
was used for statistical analysis. In preparation for telencephalic
lesions, animals were anesthetized by immersion in a solution of
tricaine methane sulfonate (1:20,000 solution p/v; Sigma, USA). The
DP(n = 7) was aspirated with a micropipette connected to a manual
vacuum system. Sham operations were performed the same way,
with the exception that the nervous tissue was not injured. The
intact group did not receive any surgical intervention. After the 5
day recovery period, the subjects were placed in the shuttle box, for
six additional sessions following the same procedure to evaluate the
degree of retention. The same variables as the pre-surgical period
were recorded. The performance during the sessions in the postsurgical period was analyzed and compared with the criteria for
each group to the pre-surgical sessions. An ANOVA with repeated
measurements was used for statistical analysis. Students t test was
used to contrast last pre-surgical session and rst post-surgical
session to analyze intra-group differences. At the end of the experiment, the sh with telencephalic lesions and sham operations
were deeply anesthetized (1:5000) and perfused with 50 mL of 0.9%
saline solution, followed by 125 mL of xative solution (10% formalin in phosphate buffer, 0.1 M, pH 7.4). The brain was removed from
the skull, inspected for a preliminary evaluation of the ablation,
and cut in transversal sections (50 m thick) for histological analysis. Graphical software was used to reconstruct the lesions onto
coronal plates adapted from the goldsh atlas of Peter and Gill [29].
2.2. Experiment 2: Trace two-way active avoidance conditioning
Fifteen experimentally naive goldsh were used in this experiment. The experimental apparatus and pre-exposure procedure
was the same as described for rst experiment. Acquisition procedure was the same to those (a daily session of 10 trials with

437

same ITI conditions). At the end of the ITI, the trial began (for a
maximum duration of 10 s), followed by a gap period of 5 s after
termination of the green light. The temporal separation between
cue onset and shock onset was 15 s. If the sh did not respond
(swimming across the barrier) within 15 s (10 s of green light plus
5 s of gap), the electric shock was turned on for a maximum of 5 s.
A response during the rst 15 s nished the green light and gap
period, and the shock was not delivered. A response during the
1520 s period canceled the shock. All conditions and learning criterion were the same as described above. All subjects reached the
criterion between sessions 11 and 19 and were randomly assigned
to one of three groups: dorsal pallium (DP) ablation (n = 8), shamoperated (n = 3), and intact (n = 4). The variables were percentage of
avoidance (shuttle responses occurring before shock onset; latency
<15 s) and percentage of escape (shuttle responses occurring during the shock; latency between 15 and 20 s). ANOVA, with repeated
measurements was used for statistical analysis. The surgical procedure was the same as for Experiment 1. After the recovery period
subjects were given six additional sessions to evaluate the degree
of retention. The same variables as in the pre-surgical period were
recorded. The performance during the sessions in the post-surgical
period was analyzed and compared with the criterion sessions in
the same way as the rst experiment. Histological analysis was
performed following the rst experiment.
3. Results
3.1. Experiment 1
Fig. 1A shows the extent of DP lesions. None of the shamoperated animals exhibited any evidence of damage to the
telencephalon or optic tectum. The dorsal pallium lesions affected
the dorsalis telencephali pars dorsalis (Dd) area completely and
parts of the dorsalis telencephali pars medialis dorsalis (Dmd) and
the dorsalis telencephali pars lateralis dorsalis (Dld) areas. Collaterally, in the more extensive lesions, parts of the telencephali pars
dorsalis centralis (Dc) area were also affected.
Once the animals reached the criterion of learning, the percentages of avoidance and escape for the six sessions of criterion level
were analyzed and compared between groups. Sham (n = 4) and
intact sh (n = 4) were pooled into a control group (n = 8) for statistical analysis because no statistically signicant differences were
observed between the sham and intact animals through the six
pre-surgical and six post-surgical sessions in either the avoidance
responses (MannWhitney test: All Us 3, n.s.; all Us 5, n.s.) or
escape (MannWhitney test: All Us 1, n.s.; all Us 4.5, n.s.). The
ANOVA analysis revealed no signicant differences between the
control and DP groups in either avoidance (F(1,13) = 2.19; n.s.) or
escape (F(1,13) = 0.41; n.s.) (Fig. 2A) during acquisition. Also there
appeared to be no signicant differences among control and DP
groups in either avoidance (F(1,13) = 2,02; n.s) or escape response
(F(1,13) = 4.5; n.s.) during the retention period (Fig. 2A). The comparison between pre-surgical and post-surgical data showed a
signicant impairment in the retention of the previously acquired
avoidance response produced by dorsal ablations (t(6) = 4,77;
p < 0.01). Consequently this group (DP) also presented signicant
differences in escape levels (t(6) = 3,75; p < 0.01) (Fig. 2A). However,
the animals nally reached a performance level similar to the control group in following ve sessions of retention. The control group
did not show any difference on neither avoidance (t(7) = 0.95; n.s.)
nor escape levels (t(7) = 0.87; n.s.) (Fig. 2A).
3.2. Experiment 2
Fig. 1B shows the lesion extent on the experimental group.
DP lesions affected mainly Dd and collaterally affected Dmd and

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J.P. Vargas et al. / Brain Research Bulletin 79 (2009) 436440

Dld. The sham-operated animals did not present any damage in

the telencephalon or optic tectum. Sham (n = 3) and intact sh
(n = 4) were pooled into a control group (n = 7) because no statistically signicant differences were observed between these groups
throughout the experiment in either avoidance (MannWhitney
test: All Us 2.5, n.s.; all Us 0, n.s.) or escape responses
(MannWhitney test: All Us 2.5, n.s.; all Us 2, n.s.). The analysis
showed no signicant differences between control and DP groups in
neither avoidance (F(1,13) = 0.27; n.s.) or escape (F(1,13) = 0.002; n.s.)
during acquisition (Fig. 2B). In contrast, during the retention phase
statistically signicant differences were found between control and
DP groups in both avoidance (F(1, 13) = 97.13; p < 0.01) and escape
responses(F(1, 13) = 49.87; p < 0.01) (Fig. 2B). DP lesion produced
a dramatic impairment in avoidance response retention (Fig. 2B).
So, intra-group analysis comparing pre- and post-surgerical performances showed statistically signicant differences for DP in both
avoidance (t(7) = 18.52; p < 0.01) and escape responses (t(7) = 4.41;
p < 0.01), but not for the control group (t(6) = 0.494; n.s.; and
(t(6) = 0.318; n.s.) (Fig. 2B).
4. Discussion

Fig. 1. This diagram represents the extent and location of the lesions of goldsh
trained in the non-trace avoidance conditioning (A) and in the trace avoidance conditioning (B). The largest (pale shading) and the smallest (dark shading) DP lesions
are showed. The borders of each telencephalic area follow the nomenclature used
elsewhere [20,29,30]. Abbreviations: ac, anterior commissure; Nt, nucleus taenia;
V, Ventral pallium; Vl, area ventralis telencephali pars lateralis; Vv, area ventralis
telencephali pars ventralis. (A) The dorsal pallium lesions affected the dorsalis telencephali pars dorsalis (Dd) area completely and parts of the dorsalis telencephali pars
medialis dorsalis (Dmd) and the dorsalis telencephali pars lateralis dorsalis (Dld)
areas. Collaterally, in the more extensive lesions, parts of the telencephali pars dorsalis centralis (Dc) region were also affected. (B) This shows lesion extention in the
experimental groups. DP lesions principally affected Dd and collaterally affected
Dmd and Dld. The numbers indicate the distance (millimeters) from the rostral pole
of the telencephalon.

The results of the present experiments show that DP lesion in

sh produces an impairment of the avoidance response in traceavoidance tasks. This impairment is similar to the one produced
after lesion to LP [30]. LP and DP lesions have produced similar
consequences on avoidance response retention, disrupting trace
learning but not non-trace [30,31]. These apparently paradoxical
similarities could evoke a suggestive discussion about actual pallial functions in teleost sh. A summary of current knowledge
about sh pallial functions, including present results, are summarized in Table 1. Thus, MP lesion disrupts emotional trace and
non-trace avoidance learning [30,31,32,35], where the emotional
factor is critical, explained in terms of the two-factor theory in
avoidance learning in sh [9]. However, it is not affected when it
is a spatial task [32,33]. LP is essential for spatial and temporal
learning but not for emotional [3032], and DP is critical whether
the main component is temporal but not when it is emotional

Fig. 2. Performance of DP and control groups during the acquisition and retention phases in experiments of non-trace avoidance conditioning (A) and trace avoidance
conditioning (B). (A) Above: Mean SEM of percentage of avoidance response during acquisition (six sessions after reaching learning criterion before surgery) and retention
(six sessions after surgery) phases; botton: Mean SEM of percentage of escape response during acquisition and retention periods. (B) Above: Mean SEM of percentage of
avoidance response during acquisition and retention phases; bottom: Mean SEM of percentage of escape response during acquisition and retention periods.

J.P. Vargas et al. / Brain Research Bulletin 79 (2009) 436440

439

Table 1
This table summarized the current knowlwedge about functional implications of sh brain pallium. Abbreviations: MP: Medial pallium; LP: Lateral pallium; DP: Dorsal
pallium; (a): acquisition; (r): retention; n.s.: No statistically signicant effects.
Pallial lesion

Spatial learning (a)

Spatial learning (r)

Non-trace avoidance learning (a)

Non-trace avoidance learning (r)

Avoidance trace learning (r)

MP
LP
DP

n.s. [32,35]
Disrupt [10,35]

n.s. [33]
Disrupt [33]
n.s. [33]

Disrupt [30,31]
n.s. [30,31]

Disrupt [30,31]
n.s. [30,31]
n.s.a

Disrupt [30,31]
Disrupt [30,31]
Disrupta

Portavella et al., present data.

or spatial (present data, [33]). Lateral, medial and dorsal pallium

of sh have been proposed as homologous of mammalian hippocampus [3,5,20,21,23], pallial amygdala [3,5,20,21] and isocortex
[4,24,25] respectively, New evidence from anatomical, developmental, and genetic markers studies supported those proposals
[22,36]. In mammals, hippocampal and prefrontal cortical lesions (a
mammal isocortical region) could disrupt learning if a temporal factor is important to solve the task [12,13,15,18,28]. In this sense, Lee
and Kesner [15] have established how hippocampus and prefrontal
cortex could be processing short-term spatial memory simultaneously. Hence, the different time-dependent involvements of these
neural structures are dissociated by the time window of memory.
Hippocampus plays a crucial role when the temporal factor is an
intermediate term, but for a short-term interval or duration even
the prefrontal cortex is enough. The results of this paper joined
to previous data about pallial functions could suggest a functional
preservation of major areas of vertebrates pallium along the evolution: MP is implicated in emotional-content learning processes like
amygdalar pallium; LP is in spatial and could be in time-content
learning processes as it is in the hippocampal system. Finally DP
could be involved in short-term memory processes in the same way
it is involved in the isocortical areas. In the case of time implications
of LP, the lesions were extended to Dld and Dlv pallial areas. Also,
Dld, Dd and Dmd have a similar pattern of connectivity [4,24,25].
Whether DP is principally drawn in short-term memory processes
as present results suggest, there is a possibility that LP time implication (short-term memory) could be reinterpreted in terms of
Dld affectation instead of Dlv. Therefore, it could be preserved as
a spatial implication exclusively for Dlv, and time functions could
be atleast shared among Dld and Dlv pallial areas. This possible
controversy could be similar to that of the mammals case. Thus,
some authors support the hypothesis of time involvements of the
hippocampal system [12,13,15,18,28]; meanwhile others claim that
the apparent time involvements could be a direct consequence of
collateral lesions on the transition cortex [19,26]. Indeed, studies
from hippocampal injury in pigeons show no time involvements.
The shape of a pigeons brain facilitates injury to the hippocampus
avoiding damage on adjacent areas of the brain [2,11,16]. Recent
studies have shown similarities and differences in vertebrate pallium development and pattern of connectivity in sh pallium,
using genetic markers of orthologous genes [36] and tracers [22]
respectively. Following these ways further analysis is necessary to
elucidate actual homologies (or analogies by its defect) among sh
brain pallium and the rest of the vertebrates. At same time, we
think it is required to perform more accurate studies of sh brain
lesion to locate specic functional pallial areas inside the larger pallial areas (MP, LP and DP). However, we consider the model of an
emotional brain with functional limbic implications, exclusively
developed from mammals (paleomammals) [17] may be revised.
Since the basic needs for species survival (i.e. recognition of environment and fast detection of good or bad consequences or
situations) would have been implemented early on in vertebrates
evolution, a sketch of the limbic system would be useful in examining the evolution of the rst vertebrates beginning 400 million
years ago. Of course, this idea is not contrary to a more sophisticated derived brain development and more accurate functional

implications of pallial telencephalon of current vertebrate brains,

which derive from primitive pallial areas of an ancestor of both
current land vertebrates and teleost sh. New evidence from future
studies could dene the limbic system as a sh brain instead of a
paleomammal brain.

Acknowledgements
This research was supported by Spanish Junta de Andaluca CVI127, SEJ2006-1713 and 2006/1284. We thank M.T. Gutirrez, for
technical assistance and Brittany Adams for her helpful comments
on the manuscript.

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