Please cite this article in press as: Durán E, et al. Lateral but not medial telencephalic pallium ablation impairs the use of goldfish spatial allocentric
strategies in a “hole-board” task. Behav Brain Res (2010), doi:10.1016/j.bbr.2010.06.010
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Lateral but not medial telencephalic pallium ablation impairs the use of goldfish
spatial allocentric strategies in a “hole-board” task
Emilio Durán
∗
, Francisco M. Oca ˜ na, Cristina Broglio, Fernando Rodríguez, Cosme Salas
Laboratory of Psychobiology, Campus Santiago Ramón y Cajal, University of Sevilla, Sevilla, Spain
article info
Article history:
Received 29 March 2010
Received in revised form 28 May 2010
Accepted 14 June 2010
Available online xxx
Keywords:
Spatial cognition
Hole-board task
Goldfish
Allocentric navigation
Telencephalon
Lateral pallium
Medial pallium
abstract
Strong evidence suggests that the ventral region of the lateral telencephalic pallium of teleost fish, a
structure involved in allocentric spatial cognition, is homologous to the hippocampus of tetrapods. This
homology was first proposed on basis of anatomical data, and subsequently confirmed by developmental,
functional and behavioural studies. Nonetheless, Saito and Watanabe [30,32] claim that not the lateral
but, rather, the medial pallium participates in goldfish spatial navigation and should be considered the
homologue of the hippocampus. Here, we further investigate the effects of selective pallial lesions on the
spatial cognition abilities of goldfish, trained in a “hole-board” analogue task, to find the baited feeder
within a 5 × 5 feeder matrix surrounded by visual cues. The task in the present experiment is similar to
that used by Saito and Watanabe, but including thorough probe tests that enabled to define clearly the
spatial strategies employed by the animals, and, therefore, the spatial deficits caused by the pallial lesions.
The results showed that the lateral, but not the medial pallium lesions, produced a dramatic impairment
in the implementation of allocentric spatial strategies. Thus, only lateral pallium lesioned goldfish, like
hippocampus lesioned tetrapods, failed to reach the goal when the cues in its proximity were excluded,
indicating that they used a guidance strategy. These results do not replicate Saito and Watanabe’s, but are
consistent to previous data indicating a close functional similarity between the lateral pallium of teleost
fish and the hippocampus of amniotes.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
The lateral telencephalic pallium (LP) of teleost fish is selectively
involved in the encoding of map-like representations as indicated
by lesion and functional studies [3,4,29,35,36,40]. For example,
lesions restricted to the LP produce severe place memory impair-
ments in goldfish trained in a plus-maze surrounded by distal visual
cues [29]. Following surgery, LP-lesioned fish show a severe and
permanent deficit in identifying a familiar place (goal location) not
only when reaching the goal requires implementing new routes
(transfer trials), but also when the familiar trajectories are available
(training trials). This impairment is as profound as that produced by
the ablation of the whole telencephalon [11,17,33,34], and seems
to affect selectively the allocentric memory system, as damage to
LP does not disrupt cue learning or other egocentrically referenced
strategies [29]. In fact, selective lesions to the dorsal (DP) or the
medial (MP) pallium do not produce any observable impairment in
spatial cognition [29]. The effects of LP lesions on goldfish spatial
∗
Corresponding author at: Laboratorio de Psicobiología, Facultad de Psicología,
C/Camilo José Cela s/n, 41018 Sevilla, Spain. Tel.: +34 954557746,
fax: +34 954557752.
E-mail address: durang@us.es (E. Durán).
performance are entirely similar to those observed in medial cor-
tex or hippocampus damaged land vertebrates trained in spatial
tasks that require the implementation of map-like representations
[1,5,10,12,14,18,19,29,35,37,39]. The role of the teleostean LP in
spatial cognition is evidenced also by the selective increase in the
transcriptive activity of the neurons in the ventral part of the lateral
telencephalic pallium of goldfish after learning a spatial constancy
task [4,40].
All these data concerning the involvement of the lateral pal-
lium of goldfish in the place memory system are consistent with
the expected topological position of the hippocampal pallium in
ray-finned fishes given that the embryonary development of the
telencephalon occurred by an eversion process. Eversion results in
the medial-to-lateral reversal of the topographical position of the
dorsal pallium zones, such that, for instance, the area equivalent
to the medial (hippocampal) pallium of evaginated telencephalons
occupies a lateral position in the telencephalic pallium of the
actinopterygian fish [2,6,7,20,21,22,23]. Particularly, the ventral
subdivision of the telencephalic pallium lateral division (Dlv) is
considered the most likely candidate as the specific homologue of
the medial pallium or hippocampus in tetrapods, on the basis of
the pattern of connectivity and other anatomical and developmen-
tal considerations [24,25,42,44]. The homology of both structures
is supported also by the similarity in the distribution pattern of
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doi:10.1016/j.bbr.2010.06.010