Serotonin receptors in cognitive behaviors

Current Opinion in Neurobiology

Volumn 7, Issue 2, 1997, Pages 243-254

  Buhot, Marie Christine ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; LIGAND; SEROTONIN; SEROTONIN ANTAGONIST; SEROTONIN RECEPTOR;

ATTENTION; BEHAVIOR; CHANNEL GATING; COGNITION; EMOTION; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; PRIORITY JOURNAL; REVIEW; SEROTONINERGIC SYSTEM; TRANSGENIC ANIMAL;

EID: 0031004070     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(97)80013-X     Document Type: Article

References (67)

1. of special interest Cassel J-C, Jeltsch H. Serotonergic modulation of cholinergic function in the central nervous system: cognitive implications. Neuroscience. 69:1995;1-41 This review is a useful examination of the extensive literature on the experimental findings (both behavioral and neurobiological) that support a role for 5-HT (and its receptors) in the modulation of cholinergic function. In particular, the authors present histological, electrophysiological, and pharmacological arguments demonstrating how the alteration of the serotonergic system induces changes in the functional integrity of the cholinergic system, which has been implicated in the control of cognitive processes. In particular, their comparative tables on the effects of pharmacological manipulation of 5-HT functions on in vitro and in vivo cholinergic release in different brain areas of the mammalian brain are valuable sources of information.
2. of special interest Steckler T, Sahgal A. The role of serotonergic - cholinergic interactions in the mediation of cognitive behaviour. Behav Brain Res. 67:1995;165-199 This is an interesting review of the recent progress in work on 5-HT and cognition. The authors present selected behavioral and neurobiological experimental arguments indicating how both serotonergic and cholinergic systems may interact or contribute, in independent ways, to cognitive behaviors. They particularly emphasize the idea that cognitive behaviors, as the final output of manipulation of the two systems, may be modified through indirect ways that control general functions, such as attention, stimulus processing and arousal. Each neurotransmitter system might thus have its own regulation to these 'biases.' A schematic representation of the neural circuits implicated in the cooperation between both neurotransmitter systems constitutes a basic element of understanding.
3. Sirviö J, Riekkinen P Jr, Jäkälä P, Riekkinen PJ. Experimental studies on the role of serotonin in cognition. Prog Neurobiol. 43:1994;363-379.
4. of outstanding interest Al-Zahrani SSA, Ho M-Y, Velazquez-Martinez DN, Lopez Cabrera M, Bradshaw CM, Szabadi E. Effect of destruction of the 5-hydroxytryptaminergic pathways on the acquisition of temporal discrimination and memory for duration in a delayed conditional discrimination task. Psychopharmacology. 123:1996;103-110 5,7-Dihydroxytryptamine lesioning of both the dorsal and the medial raphes had previously observed to disrupt acquisition and performance of temporal differentiation in rats. The authors demonstrate here that the same lesion selectively facilitates acquisition of temporal discrimination only in the experimental condition (using millisecond-range stimuli instead of seconds-range stimuli) that is acquired relatively slowly by intact rats. This is also the first study of the effect of 5-HT depletion on memory for duration.
5. Lister S, Pearce JM, Butcher SP, Collard KJ, Foster GA. Acquisition of conditioned inhibition in rats is impaired by ablation of serotoninergic pathways. Eur J Neurosci. 8:1996;415-423.
6. of special interest Santucci AC, Knott PJ, Haroutunian V. Excessive serotonin release, not depletion, leads to memory impairments in rats. Eur J Pharmacol. 295:1996;7-17 This is an original study in which the authors, using a consistent experimental design including a combination of different modes of depletion of 5-HT (i.e. PCPA and raphe lesion) and of learning models (i.e. passive avoidance and radial maze), show that 5-HT depletion has no direct effect on performance in learning and memory, whereas excessive 5-HT release (as a result, for example, of acute drug treatment) produces critical impairments, presumably through overactivation of postsynaptic receptors.
7. Menenes A, Hong E. Effect of fluoxetine on learning and memory involves multiple 5-HT systems. Pharmacol Biochem Behav. 52:1995;341-346.
8. Hoyer D, Martin GR. Classification and nomenclature of 5-HT receptors: a comment on current issues. Behav Brain Res. 73:1996;263-268.
9. 1A receptors in working memory.
10. 1A receptor antagonists, reversed this impairment.
11. 1A receptors compensate for the loss of cholinergic inputs by favoring the action of other excitatory transmitters (see annotation [13]). Nevertheless, both this study and the one described in [10] are valuable psychopharmacological protocols for the study of 5-HT receptors in learning and memory.
12. 1A receptors.
13. 1A receptors on the same target cells for which cholinergic projections are excitatory. This target probably corresponds to hippocampal pyramidal cells. This hypothesis might also be relevant for the findings of Carli et al. (see also Figure 2). This study is interesting and original in that it associates animal, lesion, and behavioral models that are particularly relevant to the analysis of cognitive decline (and recovery) in Alzheimer's disease.
14. 1A receptors involved in such effect are probably postsynaptic and located on hippocampal cells.
15. 1A agonist 8-OH-DPAT dose-dependently impaired performance (measured in terms of swim time and errors) on retention of a well learned maze, but also on acquisition of a novel configuration of the maze. This procedure of learning generalization within the framework of spatial memory is paticularly relevant to the study of the hippocampus.
16. Kinney GG, Kocsis B, Vertes RP. Medial septal unit firing characteristics following injections of 8-OH-DPAT into the median raphe nucleus. Brain Res. 708:1996;116-122.
17. Kia HK, Brisorgueil MJ, Daval G, Langlois X, Hamon M, Vergé D. Serotonin1A receptors are expressed by a subpopulation of cholinergic neurons in the rat medial septum and diagonal band of Broca - a double immunocytochemical study. Neuroscience. 74:1996;143-154.
18. 1A receptor to disinhibit CA1 pyramidal cells from interneuron inputs, probably of the GABAergic type.
19. Boschert U, Aït Amara D, Segu L, Hen R. The mouse 5-hydroxytryptamine1B receptor is localized predominantly on axon terminals. Neuroscience. 58:1994;167-182.
20. 1A agonist 8-OH-DPAT had no detrimental effect on the performance, but a facilitatory effect (i.e. decreased latency to complete trials).
21. 1B receptors located on septal cholinergic terminals.
22. 3H]acetylcholine release in hippocampal slices of rats with fimbria-fornix lesions and intrahippocampal grafts of septal origin. Brain Res. 704:1995;153-166.
23. 1B receptors, which are found in the dorsal subiculum in high density, are located on axon terminals of CA1 pyramidal cells.
24. 1B receptors induced a decrease in the release of glutamate from incoming fibers originating from CA1 pyramidal cells. This effect suppressed subicular transmission at low but not at high frequencies.
25. 1D receptor antagonist. Behav Brain Res. 73:1996;157-161.
26. 4 receptors in brain tissues from patients with neurodegenerative disorders. Behav Brain Res. 73:1996;249-252.
27. Torres GE, Chaput Y, Andrade R. Cyclic AMP protein kinase A mediate 5-hydroxytryptamine type 4 receptor regulation of calcium-activated potassium current in hippocampal neurons. Mol Pharmacol. 47:1995;191-197.
28. + current in mammalian neurons. Proc Natl Acad Sci USA. 92:1995;6635-6639.
29. 4 in memory processes, although only few behavioral experiments have been performed due to the lack of biologically stable ligands.
30. 4 receptor-mediated modulation of 5-HT release in the rat hippocampus in vivo. Br J Pharmacol. 117:1996;1475-1480.
31. Fontana DJ, Daniels SE, Eglen RM, Wong EHK. Stereoselective effects of (R)- and (S)-zacopride on cognitive performance in a spatial navigation task in rats. Neuropharmacology. 35:1996;321-327.
32. 3 receptor antagonist, on cognition in rodents and primates. Pharmacol Biochem Behav. 35:1990;955-962.
33. Fontana DJ, Daniels SE, Henderson C, Eglen RM, Wong EHF. Ondansetron improves cognitive performance in the Morris water maze spatial navigation task. Psychopharmacology. 120:1995;409-417.
34. 3 antagonist WAY-100289 on learning and memory was tested in the water maze task on rats that had sustained combined lesions of the NBM and MS. In contrast to cholinergic agonists, this treatment had no effect on acquisition, as measured before lesioning, but antagonist the retention impairment caused by the damage to both cholinergic structures.
35. 3 receptors may have an important role in modulating the functioning of both cholinergic pathways (i.e. the one originating from the NBM and projecting to cortical areas and the one originating from the MS and projecting to the hippocampus).
36. 3 receptors on hippocampal functions.
37. Morales M, Battenberg E, de Lecea L, Sanna PP, Bloom FE. Cellular and subcellular immunolocalization of the type 3 serotonin receptor in the rat central nervous system. Mol Brain Res. 36:1996;251-260.
38. Morales M, Battenberg E, de Lecea L, Bloom FE. The type 3 serotonin receptor is expressed in a subpopulation of GABAergic neurons in the rat neocortex and hippocampus. Brain Res. 731:1996;199-202.
39. 3 receptors have been located (see [38]).
40. Harvey JA. Serotonergic regulation of associative learning. Behav Brain Res. 73:1996;47-50.
41. 2A receptors inhibits the fenfluramine-induced increase of cholinergic release in the rat frontal cortex. Nevertheless, the location of this receptor on cell bodies or terminals of the NBM remains to be determined.
42. 2C serotonin receptors. Nature. 374:1995;542-546.
43. 1B receptors at the electron microscopic level.
44. 1B/1D agonist was found able to reduce distraction. This mechanism could participate to a 5-HT role in sensory gating and behavioral inhibition. It might be involved in processes underlying reactivity to the environment according to the state of arousal of the animal and/or to the salience of the stimulus.
45. Jäkälä P, Sirviö J, Jolkkonen J, Riekkinen P Jr, Acsady L, Riekkinen P. The effects of p-chlorophenylalanine-induced serotonin synthesis inhibition and muscarinic blockade on the performance of rats in a 5-choice serial reaction time task. Behav Brain Res. 51:1992;29-40.
46. Cassaday HJ, Hodges H, Gray JA. The effects of ritanserin, RU24969 and 8-OH-DPAT on latent inhibition in the rat. J Psychopharmacol. 7:1993;63-71.
47. Warburton EC, Joseph MH, Feldon J, Weiner I, Gray JA. Anatagonism of amphetamine-induced disruption of latent inhibition in rats by haloperidol and ondansentron: implications for a possible antipsychotic action of ondansetron. Psychopharmacology. 114:1994;657-664.
48. 3 receptor antagonist, ondansetron. Psychopharmacology. 118:1995;82-92.
49. Sipes TA, Geyer MA. 8-OH-DPAT disruption of prepulse inhibition in rats: reversal with (+)WAY 100, 135 and localization of site of action. Psychopharmacology. 117:1995;41-48.
50. 1B receptor knock out - behavioral consequences. Behav Brain Res. 73:1996;305-312.
51. Robbins TW, Jones GH, Wilkinson LS. Behavioral and neurochemical effects of early social deprivation in the rat. J Psychopharmacol. 10:1996;39-47.
52. 1B receptors. Pharmacol Biochem Behav. 48:1994;965-969.
53. LeDoux JE. Brain mechanisms of emotion and emotional learning. Curr Opin Neurobiol. 2:1992;191-197.
54. Gallagher M, Chiba AA. The amygdala and emotion. Curr Opin Neurobiol. 6:1996;221-227.
55. Garcia R, Jaffard R. Changes in synaptic excitability in the lateral septum associated with contextual and auditory fear conditioning in mice. Eur J Neurosci. 8:1996;809-815.
56. Wilkinson LS, Humby T, Robbins TW, Everitt BJ. Differential effects of forebrain 5-hydroxytryptamine depletions on Pavlovian aversive conditioning to discrete and contextual stimuli in the rat. Eur J Neurosci. 7:1995;2042-2052.
57. of outstanding interest Graeff FG, Viana MB, Mora PO. Opposed regulation by dorsal raphe nucleus 5-HT pathways of two types of fear in the elevated T-maze. Pharmacol Biochem Behav. 53:1996;171-177 An interesting study that attempted to dissociate, by a 'learning' (versus innate) component, two kinds of fear situations and to 'adjust' this dissociation in terms of independent underlying 5-HT pathways. The authors used an 'elevated' T-maze, in which a rat either can be placed at the end of an enclosed arm, perpendicular to two open arms, and left free to withdraw from this arm (learned fear) or can be placed at the end of one of the open arm from which it will try to escape (unconditioned fear). It was expected that afferents from the dorsal raphe to the amygdala and the frontal cortex would facilitate active escape and avoidance behavior (as conditioned or anticipatory anxiety), whereas projections from the dorsal raphe to the periaqueductal gray would inhibit inborn flight reactions arising in response to proximal danger. Lesion to the dorsal raphe facilitated learned fear and impaired unconditioned fear; d-fenfluramine treatment presented the same (but weaker) functional profile.
58. Inoue T, Tsuchiya K, Koyama T. Serotonin activation reduces defensive freezing in the conditioned fear paradigm. Pharmacol Biochem Behav. 53:1996;825-831.
59. Maier SF, Grahn RE, Watkins LR. 8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear-conditioning and interference with escape produced by exposure to inescapable shock. Behav Neurosci. 109:1995;404-412.
60. 3 receptor inactivation inhibited this effect.
61. 1A autoreceptors) on the decrease of 5-HT activity in different target structures subserving different functions. The authors also suggest that the influence of 5-HT on instrumental action would be secondary to its effects on affective arousal processes.
62. Handa RJ, George M, Gordon BH, Campbell DB, Lorens SA. Responses to novelty stress in female F344 rats: effects of age and d-fenfluramine. Pharmacol Biochem Behav. 53:1996;641-647.
63. Geyer MA. Serotonergic functions in arousal and motor activity. Behav Brain Res. 73:1996;31-35.
64. 1B receptors in the rat. Hippocampus. 5:1995;198-208 In this study, the authors used an interesting behavioral task that allowed the expression of spontaneous (cognitive and emotional) behaviors in an open field filled with different objects that could be manipulated (displaced) or replaced. Locomotor versus exploratory activities could be dissociated, as well as cognitive versus emotional exploration (i.e. increased versus decreased), respectivey, plus habituation and response to spatial versus non-spatial novelty. This behavioral task thus allowed the emergence of different patterns of behavior selectively related to the activation of different 5-HT receptors located in the CA1 field of the hippocampus.
65. Gray JA. The hippocampus as an interface between cognition and emotion. Roitblat HL, Bever TG, Terrace HS. Animal Cognition. 33:1984;607-625 Lawrence Erlbaum Associates, Hillsdale, NJ.
66. Grailhe R, Hen R. 5-HT receptor knockouts: constitutive, inducible or tissue-specific. Semin Neurosci. 7:1995;395-400.
67. Mayford M, Bach ME, Huang Y-Y, Wang L, Hawkins RD, Kandel ER. Control of memory formation through regulated expression of a CaMKII transgene. Science. 274:1996;1678-1683.