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Salud mental

versión impresa ISSN 0185-3325

Salud Ment vol.29 no.5 México sep./oct. 2006

 

Artículos originales

Dependencia de los sistemas de memoria al ciclo luz-oscuridad en la expresión de estrategias adaptativas. Segunda parte

Pavel E. Rueda-Orozco1 

Corinne J. Montes-Rodríguez1 

Edgar Soria-Gómez1 

Andrea Herrera-Solís1 

Khalil Guzmán1 

Aldebarán Prospéro-García1 

Alejandra E. Ruiz-Contreras1 

Oscar Prospéro-García1 

1Grupo de Neurociencias, Departamento de Fisiología, Facultad de Medicina, UNAM, México.

Resumen:

En la primera parte de esta revisión nos encargamos de revisar al hipocampo y al estriado en el contexto de los sistemas de memoria. En esta parte revisaremos las bases anatómicas y fisiológicas de los sistemas de memoria representados por la amígdala y la corteza prefrontal así como su participación en la expresión de estrategias para la solución de problemas específicos (estrategias adaptativas). En este apartado haremos hincapié en las funciones básicas que se le atribuyen a estas estructuras, su participación en la expresión de estrategias adaptativas y la influencia que ejercen sobre otros sistemas de memoria como el hipocampal y el estriatal. Aquí revisamos el papel de la amígdala como modulador del hipocampo y el estriado. También revisamos los conceptos de memoria de trabajo y anticipación como las principales funciones de la corteza prefrontal o neocorteza y su relación con los otros sistemas de memoria. Finalmente revisamos la bibliografía disponible acerca de los ritmos circadianos y su relación con la memoria. Haremos énfasis en la función del hipocampo. Nosotros creemos que estudiar las relaciones mencionadas puede ser una herramienta útil para comprender cómo es que el medio ambiente influencia la conducta.

Conclusiones. Cuando un sujeto es sometido a un problema determinado, éste puede solucionarlo con diferentes estrategias. La génesis y expresión de las estrategias depende de la interacción de diferentes estructuras cerebrales, entre ellas las estructuras relacionadas con los procesos de memoria. Los diferentes sistemas de memoria procesan y almacenan diferentes tipos de información. Esta información es el sustento que utiliza el cerebro, probablemente la corteza prefrontal, para la generación de las estrategias adaptativas. Por otro lado existe información que sugiere que el ciclo luz-oscuridad modula la actividad de las diferentes estructuras mencionadas. Esto implicaría que la conducta, la forma como un sujeto se adapta a su medio, estaría a su vez matizada por el ciclo luz-oscuridad.

Palabras clave: Estrategia; hipocampo; estriado; amígdala; corteza prefrontal; ciclo luz-oscuridad

Abstract:

In the first part of this work we reviewed the hippocampus and striatum anatomy and function in the context of the memory systems. In this second part we describe the anatomic and physiologic basis of the memory systems represented by the amygdala and prefrontal cortex (PFC) and their participation in the expression of strategies for the solution of specific problems. Amygdaloid formation is divided in three principal regions, the baso-lateral nucleus, the superficial nucleus, and the centromedial nucleus. Amygdala is highly connected with several regions of the brain including hippocampus, striatum and PFC. Amygdala has been implicated in the processing, storing and retrieval of emotional information.

Another function proposed for the amygdala is to modulate the activity of structures such as the hippocampus, the striatum and the cerebral cortex. The participation of the amygdala has been shown in different tasks such as the Morris water maze, the radial maze, the passive avoidance task, and the freezing behavior among others. In some of these studies it has been shown that the activation of the amygdala enhances the acquisition of the task. When the amygdala is activated pharmacologically it is able to enhance the acquisition of hippocampus or striatum related tasks. In these context, the efficiency of the amygdala activation depends on the synchrony, the precise time, at which it occurs in relation to the event the subject is learning. This is, either immediately before, during or immediately after learning.

In support of this enhancing role of the amygdala, some electrophysiological studies have shown that the activation of the amygdala facilitates the development of LTP in the hippocampus while its lesion decreases it. On the other hand, it has also been shown that the amygdala activation increases c-Fos expression in both, the hippocampus and the striatum.

In summary, the amygdaloid formation has been proposed as an enhancer of learning, representing the emotional component of the response to the environment.

PFC is the other structure involved in the generation of strategies. It has been related with the correct functioning of higher functions such as memory, attention, emotion, anticipation and planning. It has been called the central executor for its fundamental role as a coordinator of past, present information and future performance. It is been proposed as responsible for the so called working memory, that allows to put together different kinds of information at the same time, giving the chance of comparing, selecting and generating a goaloriented behavior.

Working memory has been studied with many different techniques, however electrophysiological experiments have shown interesting aspects of its functioning. Recording cells from the PFC of monkeys, Goldman-Rakic showed that these cells remain firing in a short period of time when visual information should be retained to be used in ulterior comparison task. This cell activity suggests that these neurons would be responsible for the maintenance of information in our "mind" a short period of time. These results have been replicated in humans by using real time imaging techniques as fMRI and PET. Again, during the periods of retention of the information, the activity on prefrontal areas increase until such information is used.

Besides working memory, anticipation is another important function regulated by the PFC. Several studies have shown that the activity of prefrontal cortex increases before the performance, it seems like the prefrontal cortex predicts the actions in the environment and readily generates a strategy to efficiently act in response.

PFC is connected reciprocally with the hippocampus, the striatum and the amygdala, the relation between these structures is under heavy investigation. Regarding the hippocampus, some interaction has been observed, and it has been proposed an interaction between these structures for the long term consolidation of memory. As for the striatum, the relationship with PFC has been studied preferentially with the ventral striatum or nucleus accumbens with respect to reinforcement of behavior. We understand poorly the relationship with the dorsal striatum.

The relation between amygdala and PFC, on the other hand, has been studied in relation to the expectancy of the reinforcement. This is defined as the representation in the mind of the reinforcement and the association of that representation with the conditions under which it was delivered. In simple words, this is a way to explain how is that a subject prefers a specific reinforcer over another. It has been shown that lesions of the basolateral amygdala as well as PFC interfere with the expectancy of reinforcement. The function of the amygdala in this case is to provide the emotional component related to the presence of the reinforcement.

An extensive literature has addressed the question of circadian variations in the release of neurotransmitters. For example, the diurnal variations in the release of acetylcholine in the hippocampus and PFC. The binding for acetylcholine, serotonin and norepinephrine to glutamatergic hippocampal cells is different depending on the light-dark cycle, suggesting that the modulation of the hippocampus by these neurotransmitters is different depending on the presence or absence of light.

In this review, we have devoted special interest to the influence of the light dark cycle on these mnemonic systems and on goaloriented behaviors. We analyze selected papers from the available literature on circadian rhythms and memory, emphasizing the hippocampus role. We believe that the study of this relationship (brain/light-dark cycle) could be a useful tool to understand how the environment influences behavior.

On this topic, there's evidence that the learning of a task may be different depending on the part of the day when it was learned. For example, it has been shown in humans that when subjects are submitted to explicit or implicit task the performance is different depending on the hour of the day, being better during the light for the explicit memory and better during the dark for the implicit memory. Studies in rats trained in fear conditioning tasks, showed that subjects learn the task easily when they are trained during the light phase of the cycle and the learned behavior showed a higher resistance to extinction.

Conclusión. When a subject is confronted with a specific problem, he/she can find the solution by using different strategies. The expression of one of those strategies depends on the interaction of the different memory systems, these systems process and storage different kinds of information, and this information is useful to generate and exhibit a given strategy. The memory systems are constantly under the influence of the environment, one critical component of this environment is the lightdark cycle, which apparently is modulating the activity of these structures. As a result of the influence of the light-dark cycle on these structures, the behavior of the subject would be modulated as well. All these interaction just for the sake of adaptation, survival, and reproduction in this rotating and translating world.

Key words: Strategy; hippocampus; striatum; amygdala; prefrontal cortex; light-dark cycle

Texto disponible solo en PDF

Agradecimientos

Este trabajo fue realizado con el apoyo del donativo 42060 del CONACYT, otorgado a OPG. Todas las ilustraciones son obra del licenciado Benito Moreno Gómez.

Referencias

1. Ammassari-Teule M, Marsanich B: Spatial and visual discrimination learning in CD1 mice: partial analogy between the effect of lesions to the hippocampus and the amygdala. Physiol Behav, 60:256-71, 1996. [ Links ]

2. Baddeley A: Working memory: Looking back and looking forward. Nature Reviews, 4:829-39, 2003. [ Links ]

3. Baddley A: Modulatory, mass-action and memory. Q J Exp Psychol A, 38:527-33, 1986. [ Links ]

4. Barbas H, Blatt GJ: Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus, 5: 511-33, 1995. [ Links ]

5. Boulos Z, Rosenwasser AM, Terman M: Feeding schedules and the circadian organization of behavior in the rat. Behav Brain Res, 1:39-45, 1980. [ Links ]

6. Brunel S, Montigny C: Diurnal rhytms in the responsiveness of hippocampal pyramidal neurons to serotonin, no-repinephrine, gamma aminobutyric acid and acetylcholine. Brain Res Bull, 18:205-12, 1987. [ Links ]

7. Buzsaki G: Two-stage model of memory trace formation: a role for "noisy" brain states. Neursocience, 31: 551-570, 1989. [ Links ]

8. Cauller LJ, Boulos Z, Goddard GV : Circadian rythms in hippocampal responsiveness to perforant path stimulation and their relation to behavioral state. Brain Res, 329:117-130, 1985. [ Links ]

9. Chafee MV, Goldman-Rakic PS: Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. J Neurophysiol, 83:1550-66, 2000. [ Links ]

10. Chafee MV, Goldman-Rakic PS: Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J Neurophysiol, 79:2919-40, 1998. [ Links ]

11. Chaudhury D, Colwell CS: Circadian modulation of learning and memory in fear-conditioned mice. Behav Brain Res, 133:95-108, 2002. [ Links ]

12. Courtney SM, Petit L, Maisog JM, Ungerlei-Der LG, Haxaby JV: An area specialized for working memory in human frontal cortex. Science, 279:1347-51, 1998. [ Links ]

13. Devan BD, Goad EH, Petri HL, Antoniadis EA, Hong NS, Ko CH y cols.: Circadian phase-shifted rats show normal acquisition but impaired long-term retention of place information in the water task. Neurobiol Learning Memory, 75:51-62, 2001. [ Links ]

14. Duncan J, Seitz RJ, Kolodny J, Bor D y cols.: A neural basis for general intelligence. Science, 289:457-60, 2000. [ Links ]

15. Folkard S: Diurnal variation in logical reasoning. Br J Psychol, 66:1-8, 1975. [ Links ]

16. Funahashi S, Bruce CJ, Goldman-Rakic PS: Mnemonic coding of visual space in the monkey' s dorsolateral prefrontal cortex. J Neurophysiol, 61:331-49, 1989. [ Links ]

17. Funahashi S: Neuronal mechanisms of executive control by the prefrontal cortex. Neuroscience Res, 39:147-65, 2001. [ Links ]

18. Fuster JM: Executive frontal functions. Exp Brain Res, 133:66-70, 2000. [ Links ]

19. Fuster JM: Frontal lobe and cognitive development. J Neurocytology, 31:373-85, 2002. [ Links ]

20. Fuster JM: The prefrontal cortex - An update: Time is of the essence. Neuron, 30:319-333, 2001. [ Links ]

21. Gallagher M, Kapp BS, Musty RE, Driscoll PA: Memory formation: evidence for a specific neurochemical system in the amygdala. Science, 198:423-5, 1977. [ Links ]

22. Gold PE, Sternberg DB: Retrograde amnesia produced by several treatments: evidence for a common neurobiological mechanism. Science, 201:376-9, 1978. [ Links ]

23. Goldman-Rakic PS, Selemon LD, Schwartz ML: Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocam-pal cortex in the rhesus monkey. Neuroscience, 12:719-43, 1984. [ Links ]

24. Gray TS: Fucntional and anatomical relationships among the amygdala, basal forebrain, ventral striatum, and cortex. Ann N Y Acad Sci, 29:877-44, 1999. [ Links ]

25. Harris KM, Teyler TJ: Age differences in a circadian in-fluence on hippocampal LTP. Brain Res, 261:60-73, 1983. [ Links ]

26. Holland PC, Gallager M: Amygdala-frontal interactions and reward expectancy. Curr Opinion Neurobiol, 14:148-155, 2004. [ Links ]

27. Kelley AE, Andrzejewski ME, Baldwin AE, Hernandez PJ, Wayne EP: Glutamate-mediated plasticity in corticostriatal networks. Am NY Acad Sci, 1003:159-68, 2003. [ Links ]

28. Kim JJ, Lee HJ, Han JS, Packard MG: Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci, 21:5222-8, 2001. [ Links ]

29. Kim JJ, Rison RA, Fanselow MS: Effects of amygdala, hippocampus, and periaqueductal gray lesions on short-and long-term contextual fear. Behav Neurosci, 107:1093-8, 1993. [ Links ]

30. Lorenzini CA, Bucherelli C, Giachetti, Tasso-Ni G: Conditined freezing (generalized motor inhibition) in several rat strains: its usefulness in assessing somato-vegetative responses to nocioceptive stress. Funct Neurol, 5:267-71, 1990. [ Links ]

31. Maren S, Quirk GJ. Neuronal signaling of fear memory. Nat Rev Neurosci, 5:844-52, 2003. [ Links ]

32. Maren S: Long-term potentiation in the amygdala: a mechanism for emotional learning and memory. TINS, 22:561-67, 1999. [ Links ]

33. May CP, Hasher L, Foong N: Implicit memory, age, and time of day. Psychol Sci, 16:96-100, 2005. [ Links ]

34. McDonald RJ, Hong NS: A dissociation of dorsolateral striatum and amygdala function on the same stimulus-response habit task. Neuroscience, 124:507-13, 2004. [ Links ]

35. McDonald RJ, White NM: A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behav Neurosci, 107:3-22, 1993. [ Links ]

36. McGaugh JL, McIntyre CK, Power AE: Amygdala modulation of memory consolidation with other brain systems. Neurobiol Learn Mem, 8:539-552, 2002. [ Links ]

37. McGaugh JL: Memory- a century of consolidation. Science, 287:248-251, 2000. [ Links ]

38. McGaugh JL: The amygdala modulates the consolidation of memories of emotionally arousing experiences. Anu Rev Neurosci, 27:1-28, 2004. [ Links ]

39. McIntyre CK, Power AE, Roozendaal B, McGaugh JL: Role of the basolateral amygdala in memory consolidation. Ann N Y Acad Sci, 985:273-93, 2003. [ Links ]

40. Mitsushima D, Yamanoi C, Kimura F: Restriction of enviormental space attenuates locomotor activity and hippocampal acetylcholine release in male rats. Brain Res, 805:207-12, 1998. [ Links ]

41. Mizuno T, Arita J, Kimura F: Spontaneous acetylcho-line release in the hippocampus exhibits a diurnal variation in both young and old rats. Neurosci Lett, 12:271-4, 1994. [ Links ]

42. Packard MG, Cahill L, McGaugh JL: Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc Natl Acad Sci USA, 91:8477-81, 1994. [ Links ]

43. Packard MG, Teather LA: Amygdala modulation of multiple memory systems: Hippocampus and caudate-puta-men. Neurobiol Learn Mem, 69:163-203, 1998. [ Links ]

44. Pare D: Role of the basolateral amygdala in memory consolidation. Progress Neurobiol, 70:409-20, 2003. [ Links ]

45. Parent MB, McGaugh JL: Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training. Brain Res, 661:97-103, 1994. [ Links ]

46. Passingham D, Sakai K: The prefrontal cortex and working memory: physiology and brain imaging. Curr Opinion Neurobiol, 14:163-8, 2004. [ Links ]

47. Pochon JB, Levy R, Poline JB, Crozier S y cols.: The role of dorsolateral prefrontal cortex in the preparation of forthcoming actions: an fMRI study. Cerebral Cortex, 11:260-266, 2001. [ Links ]

48. Pratt WE, Mizumori SJ: Characteristics of basolateral amygdala neuronal firing on a spatial memory task involving differential reward. Behav Neurosci, 112:554-70, 1998. [ Links ]

49. Quintana J, Fuster JM: From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cerebral Cortex, 9:213-21, 1999. [ Links ]

50. Raghavan AV, Horowitz JM, Fuller CA: Diurnal modulation of long-term potentiation in the hamster hippocampal slice. Brain Res, 833:311-4, 1999. [ Links ]

51. Ralph MR, Ko CH, Antoniadis AE, Seco P y cols.: The significance of circadian phase for performance on a reward-based learning task in hamsters. Behav Brain Res, 136:179-84, 2002. [ Links ]

52. Rosene DL, Van Hoesen GW: Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science, 1977:317-7, 1997. [ Links ]

53. Rudy JW, Huff NC, Matus-Amat P: Understanding contextual fear conditioning: insights from a two-process model. Neurosci Biobehav Rev, 28:675-685, 2004. [ Links ]

54. Rueda P, Quiroz-Torres AM, Martínez-Vargas M, Prospero-García O: Enndocanabinoid effects on memory depend on diurnal variations. 32Annual meeting of the Society for Neuroscience, Orlando, 2002. [ Links ]

55. Sah P, Faber ESL, Lopez de Armentia M, Power J: The amygdaloid complex: anatomy and physiology. Physiol Rev, 83:803-34, 2003. [ Links ]

56. Shatz C: The developing brain. Scientific American, 267:60-7, 1992. [ Links ]

57. Shoenbaum G, Chiba AA, Gallager M: Neural encoding in oprbitofrontal cortex and basolateral amygdala during ol-factory discrimination learning. J Neuroscience, 19:1876-84, 1999. [ Links ]

58. Shultz W: Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Curr Opinion Neurobiol, 14:139-47, 2004. [ Links ]

59. Sirota A, Csicsvari J, Buhl D, Buzsaki G: Comunication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci USA, 100:2065-2069, 2003. [ Links ]

60. Thierry AM, Gioanni Y, Degenetais E, Glowinski J: Hippocampo-Prefrontal cortex pathway: Anatomical and electrophysiological characteristics. Hippocampus, 10:411-419, 2000. [ Links ]

61. Vazdarjanova A, McGaugh JL: Basolateral amygdala is involved in modulating consolidation of memory for clas-sical fear conditioning. J Neurosci, 19:6615-22, 1999. [ Links ]

62. Yanovsky JA, Adler NT, Gallistel CR: Does the perception of reward magnitude of self-administered elec-trical brain stimulation have a circadian rhythm? Behav Neuroscience, 6:888-93, 1986. [ Links ]

63. Yerkes RM, Dodson JD: Te relation of strength of stimulus to rapidity of habit-formation. J Comp Neurol Psych, 18:459-482, 1908. [ Links ]

Correspondencia: Dr. Oscar Prospéro-García. Depto. de Fisiología, Fac. de Medicina, Universidad Nacional Autónoma de México. Apartado Postal 70-250, 04510, México, DF. Tel: (55) 5623 2509, Fax: (55) 5623 2395, E-mail: opg@servidor.unam.mx

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