Behavioural Brain Research 112 (2000) 85 – 97
Research report
Behavioral effects of protein deprivation and rehabilitation in
adult rats: relevance to morphological alterations in the
hippocampal formation
Nikolai V. Lukoyanov *, Jose ´ P. Andrade
Department of Anatomy, Porto Medical School, Alameda Prof. Herna ˆni Monteiro, 4200 -319 Porto, Portugal
Received 25 October 1999; received in revised form 7 February 2000; accepted 7 February 2000
Abstract
In the present study we have analyzed the behavioral and neuroanatomical effects of protein deprivation in adult rats. Starting
at 2 months of age, animals were maintained on 8%-casein diet either for 8 months (malnourished group), or for 6 months
followed by a 2-month period of nutritional rehabilitation (17%-protein diet, rehabilitated group). Malnourished rats exhibited
reduced emotional reactivity and impaired habituation in the open field. In a water maze, these animals did not differ from
controls during training, but showed retention deficits on the probe trial. However, working memory, sensorimotor abilities and
passive avoidance behavior were not significantly impaired in malnourished rats. The performance of rehabilitated group was
similar to that of the control group throughout behavioral testing. Postmortem morphological analysis revealed that the total
number of neurons in the granular layer of the dentate gyrus, and in CA3 and CA1 hippocampal fields was reduced in
protein-deprived and rehabilitated rats relative to controls. In addition, it was found that protein deprivation caused a 30% loss
of synapses established between mossy fibers and dendrites of CA3 pyramidal cells, whereas nutritional rehabilitation resulted in
a reversal of this effect. These results show that prolonged malnutrition in adult rats produces marked loss of hippocampal
neurons and synapses accompanied by substantial impairments of hippocampal-dependent behaviors. The fact that nutritional
rehabilitation results in restoration of the total number of hippocampal synapses and parallel amelioration of the behavioral
impairments suggests that the mature CNS possesses a remarkable potential for structural and functional recovery from the
damage induced by this type of dietary insult. © 2000 Elsevier Science B.V. All rights reserved.
Keywords: Long-term protein malnutrition; Open field; Passive avoidance; Morris water maze; Stereology; Neuron number; Synapse number; Rat
www.elsevier.com/locate/bbr
1. Introduction
The deleterious effects of protein malnutrition on the
developing central nervous system (CNS) have received
considerable attention both in human and animal stud-
ies [47,48,62,71]. In rodents, it has been shown that pre-
and/or early postnatal malnutrition results in long-last-
ing structural and biochemical abnormalities in differ-
ent brain regions, particularly in the neocortex and
hippocampal formation [17 – 19,21,24 – 26,52,64]. In ad-
dition, it has been repeatedly demonstrated that rats
malnourished during development exhibit numerous
and often irreversible behavioral impairments, includ-
ing alterations in avoidance [1,44], exploratory [3] and
social [2] behaviors, disturbances of emotionality
[4,36,46,69] and memory-related deficits [14–
16,22,30,39,67].
Contrary to what has been stated for decades [48,62],
there is now a growing body of evidence indicating that
prolonged protein deprivation in adulthood results in
marked structural alterations in the brain [6,7,54,56,68].
For example, it has been found that exposure of adult
rats to low-protein diet for 6 months produces massive
neuronal loss in the dentate gyrus, CA3 and CA1
* Corresponding author. Tel.: +351-22-5096808; fax: +351-22-
5505640.
E-mail address: luk@med.up.pt (N.V. Lukoyanov)
0166-4328/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved.
PII:S0166-4328(00)00164-9