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Effects of a brief sensorimotor training on the development of behavioral inhibition in the mouse
Behavioural Processes 39 (1997) 295 – 298
Short report
Effects of a brief sensorimotor training on the development of behavioral inhibition in the mouse J. Caston*, J. Lateurte Uni6ersite´ de Rouen, Faculte´ des Sciences, Laboratoire de Neurophysiologie sensorielle, 76821 Mont-Saint-Aignan Cedex, France Received 26 February 1996; revised 5 September 1996; accepted 5 September 1996
Abstract In the young C57Bl6 mouse, the hyperexcitability phase (‘pop-corn’ stage) which normally occurs around the 16–18th postnatal day and lasts 3–6 days, was greatly shortened by an intensive sensorimotor training when the ‘pop-corn’ stage appeared. It was prevented when the animals were trained for 4 days before it appeared. This might suggest, at least in part, that an early short duration sensorimotor training increased the rate of maturation of the inhibitory systems that sustain the development of the motor behavior. © 1997 Elsevier Science B.V. Keywords: Development; Hyperexcitability; Inhibition; Mouse; Training
1. Introduction The evolution of the spontaneous locomotor activity during ontogenesis depends on the level of maturation of the nervous system. Oakley and Plotkin (1975) have demonstrated that this evolution was different in rats, guinea pigs and rabbits, three species whose neural maturation is different at birth. Particularly, these authors confirm the existence of a close correlation between the peak * Corresponding author. Tel.: +33 5 146722; fax: +33 5 146349.
of motor activity and the maturation of the mesencephalic arousal stuctures (mesencephalic reticular formation) as well as between the decrease of the spontaneous activity and the maturation of descending inhibitory systems from the telencephalon. However, the nervous system does not maturate independently of the environment in which the animal develops and a great number of studies have demonstrated the role of early experience in the maturation of nervous structures and motor behavior. Early tactile (Labarba et al., 1974) and vestibular stimulations (Hard and Larsson, 1975; Clark et al., 1977; Hoffman et al.,
0376-6357/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S 0 3 7 6 - 6 3 5 7 ( 9 6 ) 0 0 7 5 4 - 1
296
J. Caston, J. Lateurte / Beha6ioural Processes 39 (1997) 295–298
1978; Ornitz, 1983) seem to be crucial in the development of motor behavior. The aim of the present work was to study, in C57Bl6 mouse, the role of early sensorimotor experience in the evolution of the hyperexcitability stage which appears between postnatal days 16 and 18 and lasts 3 – 6 days. Such a behavior results in excessive and disorderly jumps in their cage when the animals are submitted to auditory or vibratory stimuli, a behavior resembling that of corn in a frying-pan (pop-corn stage) (Sax et al., 1968; Guastavino, 1988). It might be correlated with a high mesencephalic arousal activity and is likely to disappear when inhibitory systems are developing. The present experiment may therefore represent a behavioral test of the maturation of the inhibitory structures.
2. Materials and methods The animals were C57Bl6 mice born in the laboratory and housed with their mother until weaning in standard conditions (12 h light – 12 h dark, 20–22°C). The day of birth (day 1) was exactly known by inspection of the cages twice daily. 53 mice belonging to seven different litters were divided into four groups: two experimental groups (E1, n=12: six males and six females, and E2, n= 10: five males and five females) and two controls (C1, n =16: eight males and eight females and C2, n =15, eight males and seven females). The litters ranged from 6 – 10 mice (mean 9S.D.= 7.6 91.3) and each group was composed from at least four litters to avoid the litter effects bias. The mice of the experimental groups were subjected, in the morning, to a sensorimotor training on a rotorod, which consisted in 10 daily rotations at the rate of 20 revolutions per min. In E1 mice, training began when the ‘popcorn’ stage appeared (from day 17 or 18, depending on the animals) and was stopped when it could no longer be elicited, to know whether training could influence the duration of the hyperexcitability stage. In E2 mice, training began before the ‘pop corn’ stage appeared (from day 15) to see whether sensorimotor training could prevent its appearance. Each trial, which lasted until
the animals fell down, allowed a lot of sensory stimulations (vestibular, proprioceptive, tactile) that the animals need to maintain balance. Control mice, belonging to the same litters as the experimental animals, were not subjected to the sensorimotor training. Their only experience (to which the experimental animals were also similarly subjected) was handling made necessary when cleaning the housing cages. The evolution of the ‘pop-corn’ behavior with age was seen by eye. This behavior was initiated by auditory (hand-clap) or vibratory (tapping on the support) stimulations. For this purpose, the ‘pop corn’ reaction was elicited just before the rotorod training and 1 h after in the housing cage of the animals that contained the experimental and the control mice of the same litter. Both groups were recognized by indelible color dashes painted on the tail. The ages when the ‘pop-corn’ stage appeared and disappeared were carefully noted and the mean age when it vanished was calculated in each group. Useful comparisons were made with ANOVA.
3. Results A total of 12 experimental mice (E1) were subjected to a daily training on the rotorod from day 17 or 18, when the ‘pop-corn’ behavior just appeared. At that time, they maintained balance for 92.49 19.6 s. The hyperexcitability had completely disappeared at the mean age of 18.19 0.2 days, that is by the end of the first ten trials (seven animals) or the day after (five animals). Indeed, when they were put into their cage together with the control mice of the same litters, they were the only animals which failed to exhibit the hyperexcitability to auditory and vibratory stimuli. The pop-corn stage of controls, which lasted until day 23–24 (mean age: 23.29 0.1 days) was significantly longer than that of trained mice (df= 1– 26, F= 363.782; P B 0.001). Ten other mice (E2) were subjected to a daily training on the rotorod from day 15 (before the pop-corn behavior appeared) to day 18. They maintained balance for 13.69 4.1 s at day 15,
J. Caston, J. Lateurte / Beha6ioural Processes 39 (1997) 295–298
24.19 5.7 s at day 16, 57.8 9 18.4 s at day 17 and 141.39 25.6 s at day 18. Following such a training, the hyperexcitability stage failed to appear while, in all the controls of the same litters, it was obvious from day 17 or 18 and lasted 4 – 5 days.
4. Discussion The results of the present study demonstrate the effects of sensorimotor training on the hyperexcitability stage in C57Bl6 mice. During training, the mice were subjected to an intensive complex experience including handling, vestibular, tactile and proprioceptive stimulations. The decrease of the ‘pop corn’ stage when the animals were trained once it began to appear, or the fact that it was prevented when the animals were trained before it appeared, can be explained in several ways. One can consider that the hyperexcitability stage represents an emotional behavior; in this case, a decrease of emotivity by repeated handling, could well explain the results of the present study. One can also think that the maturation rate of the sensory systems involved in rotorod training is accelerated as it has been demonstrated for long that environmental stimuli increase the maturation of the nervous system (Jeannerod and He´caen, 1979). If so, the increase of maturation rate of the sensory systems which are needed for a proper motor behavior could be responsible, at least partially, for the decrease or the lack of the hyperexcitability stage. At last, it can be considered that the pop corn stage is a diffuse motor behavior which its’ decrease is due to the maturation of the telencephalic inhibitory systems (Oakley and Plotkin, 1975). If such a view is correct, the results obtained in the present study suggest that a very brief but intensive sensorimotor training was able to increase this maturation rate. This is in agreement with Hard and Larsson (1975) who demonstrated that the maturation of the righting reflex was accelerated by a brief training for a few hours before the test and the studies of Dufour-Mallet et al. (1979) and, Auvray et al. (1989) also showed that training on the rotorod increased the rate of the maturation of balance. However, in the above-mentioned studies, the re-
297
action whose maturation was accelerated was that which was trained (righting reflex or equilibrium behavior, respectively). In the present study, training had a much more general effect since the behavior whose maturation was accelerated (spontaneous motor behavior as a whole and decreased excitability), was different from that which was trained (equilibrium behavior specifically). In that way, our results also agree with those of Labarba et al. (1974) who showed that the activity was greater in adult mice which were submitted to a 2 min daily tactile stimulation from the day of birth to the 10th postnatal day than in controls, as well as with the study of Clark et al. (1977) who demonstrated that semicircular canal stimulation in preambulatory infants accelerated motor development (motor reflexes as well as motor skills). They also agree with the fact that vestibular stimulations can facilitate behavior improvement in hyperkinetic children (Bhatara et al., 1981). It is interesting to note that the pop-corn behavior was never observed in young rats, suggesting that the maturation of the rat’s inhibitory nervous structures was achieved before that of the mouse. Such interspecific differences in the maturation rate of inhibitory systems were previously mentioned by Oakley and Plotkin (1975).
References Auvray, N., Caston, J., Reber, A. and Stelz, T., 1989. Role of the cerebellum in the ontogenesis of the equilibrium behavior in the young rat: a behavioral study. Brain Res., 516: 104 – 110. Bhatara, V., Clark, D.L., Arnold, L.E., Gunsett, R. and Smeltzer, D.J., 1981. Hyperkinesis treated by vestibular stimulation: an exploratory study. Biol. Psychiatry, 16: 269 – 279. Clark, D.L., Kreutzberg, J.R. and Chee, F.K.W., 1977. Vestibular stimulation influence on motor development in infants. Science, 196: 1228 – 1229. Dufour-Mallet, A., Caston, J. and Parrad, J., 1979. Ontogeny of equilibrium behavior in the rat with special reference to the influence of vision and training. Physiol. Behav., 22: 883 – 894. Guastavino, J.M., 1988. Ethoge´ne`se de la souris mutante staggerer: Facteurs e´pige´ne´tiques et re´cupe´rations fonctionnelles. The`se de Doctorat d’Etat, Universite´ Paris Nord, France, pp. 217.
J. Caston, J. Lateurte / Beha6ioural Processes 39 (1997) 295–298
298
Hard, E. and Larsson, K., 1975. Development of air righting in rats. Brain Behav. Evol., 11: 53–59. Hoffman, R.B., Salinas, G.A., Boyd, J.F., von Baumgarten, R.J. and Baky, A.A., 1978. Effect of prehatching weightlessness on adult fish behavior in dynamic environments. Aviat. Space Environ. Med., 49: 576–581. Jeannerod, M. and He´caen, H., 1979. Adaptation et restauration des fonctions nerveuses. Simep, Villeurbanne. Labarba, R.C., Fernandez, B., White, J.L. and Stewart, A., 1974. The effects of neonatal tactile stimulation on adult emotional
.
reactivity in BALB/c mice. Dev. Psychobiol., 7: 393 – 398. Oakley, D.A. and Plotkin, H.C., 1975. Ontogeny of the spontaneous locomotor activity in rabbit, rat and guinea pig. J. Comp. Physiol. Psychol., 89: 267 – 273. Ornitz, E.M., 1983. Normal and pathological maturation of vestibular function in the human child. In: R. Romand (Editor), Development of Auditory and Vestibular Systems, Academic Press, New York, pp. 479 – 536. Sax, D.S., Hirano, A. and Shofer, R.J., 1968. Staggerer, neurological murine mutant. Neurology, 18: 1093 – 1100.
Short report
Effects of a brief sensorimotor training on the development of behavioral inhibition in the mouse J. Caston*, J. Lateurte Uni6ersite´ de Rouen, Faculte´ des Sciences, Laboratoire de Neurophysiologie sensorielle, 76821 Mont-Saint-Aignan Cedex, France Received 26 February 1996; revised 5 September 1996; accepted 5 September 1996
Abstract In the young C57Bl6 mouse, the hyperexcitability phase (‘pop-corn’ stage) which normally occurs around the 16–18th postnatal day and lasts 3–6 days, was greatly shortened by an intensive sensorimotor training when the ‘pop-corn’ stage appeared. It was prevented when the animals were trained for 4 days before it appeared. This might suggest, at least in part, that an early short duration sensorimotor training increased the rate of maturation of the inhibitory systems that sustain the development of the motor behavior. © 1997 Elsevier Science B.V. Keywords: Development; Hyperexcitability; Inhibition; Mouse; Training
1. Introduction The evolution of the spontaneous locomotor activity during ontogenesis depends on the level of maturation of the nervous system. Oakley and Plotkin (1975) have demonstrated that this evolution was different in rats, guinea pigs and rabbits, three species whose neural maturation is different at birth. Particularly, these authors confirm the existence of a close correlation between the peak * Corresponding author. Tel.: +33 5 146722; fax: +33 5 146349.
of motor activity and the maturation of the mesencephalic arousal stuctures (mesencephalic reticular formation) as well as between the decrease of the spontaneous activity and the maturation of descending inhibitory systems from the telencephalon. However, the nervous system does not maturate independently of the environment in which the animal develops and a great number of studies have demonstrated the role of early experience in the maturation of nervous structures and motor behavior. Early tactile (Labarba et al., 1974) and vestibular stimulations (Hard and Larsson, 1975; Clark et al., 1977; Hoffman et al.,
0376-6357/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S 0 3 7 6 - 6 3 5 7 ( 9 6 ) 0 0 7 5 4 - 1
296
J. Caston, J. Lateurte / Beha6ioural Processes 39 (1997) 295–298
1978; Ornitz, 1983) seem to be crucial in the development of motor behavior. The aim of the present work was to study, in C57Bl6 mouse, the role of early sensorimotor experience in the evolution of the hyperexcitability stage which appears between postnatal days 16 and 18 and lasts 3 – 6 days. Such a behavior results in excessive and disorderly jumps in their cage when the animals are submitted to auditory or vibratory stimuli, a behavior resembling that of corn in a frying-pan (pop-corn stage) (Sax et al., 1968; Guastavino, 1988). It might be correlated with a high mesencephalic arousal activity and is likely to disappear when inhibitory systems are developing. The present experiment may therefore represent a behavioral test of the maturation of the inhibitory structures.
2. Materials and methods The animals were C57Bl6 mice born in the laboratory and housed with their mother until weaning in standard conditions (12 h light – 12 h dark, 20–22°C). The day of birth (day 1) was exactly known by inspection of the cages twice daily. 53 mice belonging to seven different litters were divided into four groups: two experimental groups (E1, n=12: six males and six females, and E2, n= 10: five males and five females) and two controls (C1, n =16: eight males and eight females and C2, n =15, eight males and seven females). The litters ranged from 6 – 10 mice (mean 9S.D.= 7.6 91.3) and each group was composed from at least four litters to avoid the litter effects bias. The mice of the experimental groups were subjected, in the morning, to a sensorimotor training on a rotorod, which consisted in 10 daily rotations at the rate of 20 revolutions per min. In E1 mice, training began when the ‘popcorn’ stage appeared (from day 17 or 18, depending on the animals) and was stopped when it could no longer be elicited, to know whether training could influence the duration of the hyperexcitability stage. In E2 mice, training began before the ‘pop corn’ stage appeared (from day 15) to see whether sensorimotor training could prevent its appearance. Each trial, which lasted until
the animals fell down, allowed a lot of sensory stimulations (vestibular, proprioceptive, tactile) that the animals need to maintain balance. Control mice, belonging to the same litters as the experimental animals, were not subjected to the sensorimotor training. Their only experience (to which the experimental animals were also similarly subjected) was handling made necessary when cleaning the housing cages. The evolution of the ‘pop-corn’ behavior with age was seen by eye. This behavior was initiated by auditory (hand-clap) or vibratory (tapping on the support) stimulations. For this purpose, the ‘pop corn’ reaction was elicited just before the rotorod training and 1 h after in the housing cage of the animals that contained the experimental and the control mice of the same litter. Both groups were recognized by indelible color dashes painted on the tail. The ages when the ‘pop-corn’ stage appeared and disappeared were carefully noted and the mean age when it vanished was calculated in each group. Useful comparisons were made with ANOVA.
3. Results A total of 12 experimental mice (E1) were subjected to a daily training on the rotorod from day 17 or 18, when the ‘pop-corn’ behavior just appeared. At that time, they maintained balance for 92.49 19.6 s. The hyperexcitability had completely disappeared at the mean age of 18.19 0.2 days, that is by the end of the first ten trials (seven animals) or the day after (five animals). Indeed, when they were put into their cage together with the control mice of the same litters, they were the only animals which failed to exhibit the hyperexcitability to auditory and vibratory stimuli. The pop-corn stage of controls, which lasted until day 23–24 (mean age: 23.29 0.1 days) was significantly longer than that of trained mice (df= 1– 26, F= 363.782; P B 0.001). Ten other mice (E2) were subjected to a daily training on the rotorod from day 15 (before the pop-corn behavior appeared) to day 18. They maintained balance for 13.69 4.1 s at day 15,
J. Caston, J. Lateurte / Beha6ioural Processes 39 (1997) 295–298
24.19 5.7 s at day 16, 57.8 9 18.4 s at day 17 and 141.39 25.6 s at day 18. Following such a training, the hyperexcitability stage failed to appear while, in all the controls of the same litters, it was obvious from day 17 or 18 and lasted 4 – 5 days.
4. Discussion The results of the present study demonstrate the effects of sensorimotor training on the hyperexcitability stage in C57Bl6 mice. During training, the mice were subjected to an intensive complex experience including handling, vestibular, tactile and proprioceptive stimulations. The decrease of the ‘pop corn’ stage when the animals were trained once it began to appear, or the fact that it was prevented when the animals were trained before it appeared, can be explained in several ways. One can consider that the hyperexcitability stage represents an emotional behavior; in this case, a decrease of emotivity by repeated handling, could well explain the results of the present study. One can also think that the maturation rate of the sensory systems involved in rotorod training is accelerated as it has been demonstrated for long that environmental stimuli increase the maturation of the nervous system (Jeannerod and He´caen, 1979). If so, the increase of maturation rate of the sensory systems which are needed for a proper motor behavior could be responsible, at least partially, for the decrease or the lack of the hyperexcitability stage. At last, it can be considered that the pop corn stage is a diffuse motor behavior which its’ decrease is due to the maturation of the telencephalic inhibitory systems (Oakley and Plotkin, 1975). If such a view is correct, the results obtained in the present study suggest that a very brief but intensive sensorimotor training was able to increase this maturation rate. This is in agreement with Hard and Larsson (1975) who demonstrated that the maturation of the righting reflex was accelerated by a brief training for a few hours before the test and the studies of Dufour-Mallet et al. (1979) and, Auvray et al. (1989) also showed that training on the rotorod increased the rate of the maturation of balance. However, in the above-mentioned studies, the re-
297
action whose maturation was accelerated was that which was trained (righting reflex or equilibrium behavior, respectively). In the present study, training had a much more general effect since the behavior whose maturation was accelerated (spontaneous motor behavior as a whole and decreased excitability), was different from that which was trained (equilibrium behavior specifically). In that way, our results also agree with those of Labarba et al. (1974) who showed that the activity was greater in adult mice which were submitted to a 2 min daily tactile stimulation from the day of birth to the 10th postnatal day than in controls, as well as with the study of Clark et al. (1977) who demonstrated that semicircular canal stimulation in preambulatory infants accelerated motor development (motor reflexes as well as motor skills). They also agree with the fact that vestibular stimulations can facilitate behavior improvement in hyperkinetic children (Bhatara et al., 1981). It is interesting to note that the pop-corn behavior was never observed in young rats, suggesting that the maturation of the rat’s inhibitory nervous structures was achieved before that of the mouse. Such interspecific differences in the maturation rate of inhibitory systems were previously mentioned by Oakley and Plotkin (1975).
References Auvray, N., Caston, J., Reber, A. and Stelz, T., 1989. Role of the cerebellum in the ontogenesis of the equilibrium behavior in the young rat: a behavioral study. Brain Res., 516: 104 – 110. Bhatara, V., Clark, D.L., Arnold, L.E., Gunsett, R. and Smeltzer, D.J., 1981. Hyperkinesis treated by vestibular stimulation: an exploratory study. Biol. Psychiatry, 16: 269 – 279. Clark, D.L., Kreutzberg, J.R. and Chee, F.K.W., 1977. Vestibular stimulation influence on motor development in infants. Science, 196: 1228 – 1229. Dufour-Mallet, A., Caston, J. and Parrad, J., 1979. Ontogeny of equilibrium behavior in the rat with special reference to the influence of vision and training. Physiol. Behav., 22: 883 – 894. Guastavino, J.M., 1988. Ethoge´ne`se de la souris mutante staggerer: Facteurs e´pige´ne´tiques et re´cupe´rations fonctionnelles. The`se de Doctorat d’Etat, Universite´ Paris Nord, France, pp. 217.
J. Caston, J. Lateurte / Beha6ioural Processes 39 (1997) 295–298
298
Hard, E. and Larsson, K., 1975. Development of air righting in rats. Brain Behav. Evol., 11: 53–59. Hoffman, R.B., Salinas, G.A., Boyd, J.F., von Baumgarten, R.J. and Baky, A.A., 1978. Effect of prehatching weightlessness on adult fish behavior in dynamic environments. Aviat. Space Environ. Med., 49: 576–581. Jeannerod, M. and He´caen, H., 1979. Adaptation et restauration des fonctions nerveuses. Simep, Villeurbanne. Labarba, R.C., Fernandez, B., White, J.L. and Stewart, A., 1974. The effects of neonatal tactile stimulation on adult emotional
.
reactivity in BALB/c mice. Dev. Psychobiol., 7: 393 – 398. Oakley, D.A. and Plotkin, H.C., 1975. Ontogeny of the spontaneous locomotor activity in rabbit, rat and guinea pig. J. Comp. Physiol. Psychol., 89: 267 – 273. Ornitz, E.M., 1983. Normal and pathological maturation of vestibular function in the human child. In: R. Romand (Editor), Development of Auditory and Vestibular Systems, Academic Press, New York, pp. 479 – 536. Sax, D.S., Hirano, A. and Shofer, R.J., 1968. Staggerer, neurological murine mutant. Neurology, 18: 1093 – 1100.