Resumen:

Una de las más importantes funciones del sistema circadiano es asegurar que las variables fisiológicas y conductuales se ajusten apropiadamente a las señales ambientales periódicas, fenómeno denominado sincronización. Por medio de este mecanismo, muchas especies adoptan un nicho temporal que complementa a su nicho espacial. De este modo, los mamíferos pueden ser nocturnos, diurnos o crepusculares, o bien pueden confinar su actividad a tiempos limitados del día. En algunas condiciones, los estímulos sincronizadores pueden generar una aparente sincronización del organismo a su ambiente. En estas circunstancias, el estímulo actúa directamente sobre los efectores del reloj biológico sin afectarlo, fenómeno llamado enmascaramiento. De tal modo, las señales ambientales periódicas tienen un efecto dual sobre los ritmos circadianos. En 1978, Aschoff describió: “Una de las dificultades de analizar la sincronización de un reloj biológico a una señal ambiental es el hecho de que el sincronizador no afecta sólo al reloj biológico, sino que usualmente afecta también a los efectores del mismo, que expresan el ritmo biológico”. Por lo anterior, se puede considerar que los efectos del enmascaramiento son una consecuencia natural e inevitable de la vida en ambientes rítmicos. De tal forma, los ritmos biológicos expresados por los efectores del reloj biológico son una mezcla de efectos debidos al enmascaramiento y de aquéllos de un sistema temporal interno del animal. Existe una importante diferencia entre el patrón temporal de expresión de un ritmo sincronizado y uno enmascarado. Cuando una señal ambiental periódica enmascara un ritmo biológico, el curso temporal es muy similar, mas no idéntico, a cuando un ritmo circadiano se sincroniza a la misma señal ambiental. En el caso de un ritmo enmascarado, la transición entre los dos estados conductuales es abrupta como el cambio en la señal ambiental. En cambio cuando el ambiente actúa como sincronizador, la transición conductual es gradual y la relación de fase entre la señal ambiental periódica y el ritmo circadiano es inexacta. Existen dos procesos que compiten por el control de los efectores (osciladores periféricos) que expresan a los ritmos circadianos en un organismo: un proceso inhibitorio que está relacionado con una iluminación brillante (enmascaramiento negativo) y un proceso estimulatorio relacionado con una iluminación muy tenue, debajo de 1 lux (enmascaramiento positivo). La reducción inmediata de la liberación de la melatonina, por la acción de la luz sobre la glándula pineal, y la inhibición de la actividad locomotora, en roedores nocturnos después de un pulso de luz en la noche, son ejemplos de esto. Los límites de sensibilidad espectral necesariospara generar la inhibición en la síntesis y la liberación de melatonina y de la actividad locomotora, en ratas y hamsters, sugieren la participación de fotorreceptores tipo bastones, esto es el fotorreceptor predominante en la retina del roedor. Sin embargo, los ratones mutantes rd/rd, muestran una supresión de la liberación de la melatonina y de la actividad locomotora después de un pulso luz. Esto sugiere que los fotorreceptores tipo conos y bastones no son necesarios para mediar los efectos agudos de la luz sobre la síntesis y la liberación de melatonina y de la actividad locomotora y que el enmascaramiento a la luz depende de otro tipo de fotorreceptor contenido en la retina. La lesión del NSQ induce la pérdida de diferentes ritmos circadianos en ciclos de luz-oscuridad (L:O). Otros trabajos reportan, en cambio, la persistencia del enmascaramiento inducido por la luz en condiciones de L:O después de la lesión del NSQ. La lesión de otras estructuras del sistema visual del roedor altera la respuesta de enmascaramiento a la luz. De hecho, la lesión de la IGL y de la corteza visual induce un aumento significativo del enmascaramiento en hamsters y ratones. A los ratones mutantes del gen CLOCK, pulsos de luz brillante, entre 100 a 1600 lux, inducen una disminución de la actividad locomotora del sujeto, pero no la suspenden completamente. Por otro lado, pulsos de luz tenue inducen un incremento de los niveles basales de la actividad locomotora (enmascaramiento positivo) de manera similar a los sujetos normales. No ha sido determinada la participación de otros genes reloj en la regulación del enmascaramiento a la luz.

Palabras clave: Enmascaramiento a la luz; sincronización; ritmos biológicos; reloj biológico

Abstract:

Organisms adapt their temporary niche with two complementary mechanisms. The first mechanism is referred to as entrainment of the endogenous biological clock, which circumscribes temporarily the activity of the subject into day or night. The second mechanism is defined as masking, and this refers to an alternative route which does not involve the activity of the pacemaker. It involves, instead, a sharp response of the animal during light-time, inhibiting or enhancing the expression of locomotor activities in nocturnal or diurnal species, respectively. Masking describes the direct and immediate effects on the expression of any biological rhythm induced by the season-dependent signals present in the environment. Moreover, this masking mechanism appears to complement the biological clock entrainment, which is used by organismsto adapt to their specific nocturnal or diurnal niche. Several constraints arise when trying to study the biological clock entrainment or the light-associated oscillators system. Theseare due to the fact that the zeitgeber influences the biological clock and affects the output response of the circadian clock. According to the aforementioned description, it appears the masking effects occur as a natural event and result from an inevitable consequence to the season-dependent life of living organisms. Circadian rhythms do not only reflect the physiological output responses of the biological clocks as their activities also result from a mixture of responses arising either from the masking effects and/or from the entrainment mechanisms driving the timing of the biological clock within the animal. Although conspicuous differences do exist between maskingand entrained- rhythms, both rhythms follow a similar timecourse. Nevertheless, the transition between light and darkness (environmental change) under the masking rhythm results in abrupt changes in the animal behavior activity (i.e, from a resting to an ambulatory activity or viceversa). In contrast, when the environment acts as a zeitgeber under the biological clock entrainment, the behavioural transition of the animal appears to be less abrupt and, therefore, the environment factors affecting the biological rhythms never match. Based on different chronobiological studies in animals, several authors have described different forms of masking mechanisms used by the brain, and classified according to the light-induced decrease or increase locomotor activity responses: a) Positive Masking refers to the increase or decrease of locomotor activity response in a diurnal or nocturnal animal, respectively, as a result of the increase in lighting; b) Negative Masking refers to the decrease of locomotor activity responses as a result of decrease in lighting in a diurnal animal, or an increase in lighting in a nocturnal animal; c) Paradoxical Positive Masking refers either to the increase locomotor activity responses of a nocturnal animal exposed to increase lighting or an increase in locomotor activity responses in a diurnal animal after lighting decreases; d) Paradoxical Negative Masking refers to the decrease of locomotor activity responses in a nocturnal animal when lighting is decreased, or to the decrease of locomotor activity responses in a diurnal animal when lighting is increased. In addition to the aforementioned classification of different masking mechanisms on the behavioral locomotor activity responses in both diurnal and nocturnal animals, other authors classify different forms of masking, based on the neural mechanisms that generate the masking effects. Authors defined the occurence of different forms of masking effects when enviromental factors (i.e, light, darkness) produce direct or indirect effects on the cyrcadian rhythm in an animal. Thus, a) Type I masking occurs when the environment produces a direct effect on the circadian rhythm output; b) Type II masking occurs when behavioral changes in the animal affect other physiological brainrhythms, for instance, an increase or decrease of behavioral locomotor activity may affect the temperature rhythm of an organism, enhancing the expression of an altered activity on the biological clock; c) Type III masking occurs when physiological or biochemical changes alter the neural output of the biological clock that conveys the time-related information of the biological rhythm; for instance, physiological or pathological conditions have been shown to affect the functional activity of specific neural pathways and their membrane receptors involved in the regulation of the body temperature. Such situations appear to modify the phase of the body temperature rhythm with the phase of the biological clock, which both rhythms appear to match under basal conditions.

The sensibility limits necessary to generate the inhibition of the synthesis and release of melatonine, in rats and hamster, suggest the involvement of the rods, the predominant photoreceptor in the rodent retina. Nevertheless, studies the mutant mice rd/rd (the mutation rd generates the total loss of photoreceptors type rods and a considerable loss of photoreceptors type cones) presented an inhibition in the synthesis and release of the melatonine and locomotor activity induced by the light. This suggests that the photoreceptors type cones and rods are not necessary to mediate the effects of the light on the locomotor activity and that the light masking depends on another type of contained photoreceptor in the retina. Some studies report the loss of the rhythmycity in drinking, locomotion or sleep-wakefulness, not only when the animals are kept in light constant, also when the animals are kept under lightdarkness cycles (L:D). Other studies that involve to mutant mice of the two genescryptocromos, which they are arrhythmic in constant conditions; they show a SCN functional diminished, light pulses applied in the subjective night do not generate alterations in the inhibition of the locomotor activity induced by the light. This suggests the loss of the masking responses induced by light. Certainly, these results point to a loss or attenuation of the masking by the SCN lesion. On the other hand, other works showing a persistence of the masking pd drinking and locomotor activity in L:D conditions after the SCN lesions. The lesions of other structures of the rodent visual system alter the light masking. It is more a significant increase of the masking in subjects with IGL lesion is observed. Subsequently, it was reported that the masking induced by the light was more significant in mice that were submitted to an NGLd lesions, which suggests that the increase in the masking to the light observed after the IGL lesions are probably due to an incidental damage of the NGLd. It also has been reported that the light masking increase after the visual cortex lesions in hamster and mice. The mutant mice clock shows brilliant light pulses: between 100 to 1600 lux they induce a complete suppression of the locomotor activity (negative masking). On the other hand, dim light pulses induce an increment of the basal levels of the locomotor activity (positive masking) in a similar way to that of the normal subjects. The participation of other genes clock in the regulation of the light-masking has not been specific. The masking is not a limited phenomenon to conditions of laboratory. There are few examples of the direct effects of light on the temporary organization of the behavior in wildlife. An impressive case is the owl primate (Aotus lemurinus griseimembra), which shows a pattern of locomotor activity that depends on the lunar cycle. This primate is nocturnal, but its activity increases (positive masking) when the luminescence is found between 0.1 and 0.5 lux, the luminescence generated precisely by the brightness of the moon. Intensities of light lower to this diminish the locomotor activity (negative masking) of the subject. The masking mechanism is an important process in the adaptation of an organism to its environment as it confers this the capacity to respond quickly to a sudden change in environmental conditions. Since the functional point of view the masking contributes to an increment in the amplitude of a entrainment rhythm, promotes direct responses to geophysical variables that the organism selects that they optimize its evolution and its adaptation to its temporary niche, all this contributes to an increase in the probability of survival of the subject to its environment.

Key words: Masking; biological rhythms; photic entrainment and biological clock