The Role of the Intergeniculate Leaflet in Entrainment of Circadian Rhythms to a Skeleton Photoperiod

Mammalian circadian rhythms are synchronized to environmental light/dark (LD) cycles via daily phase resetting of the circadian clock in the suprachiasmatic nucleus (SCN). Photic information is transmitted to the SCN directly from the retina via the retinohypothalamic tract (RHT) and indirectly from the retinorecipient intergeniculate leaflet (IGL) via the geniculohypothalamic tract (GHT). The RHT is thought to be both necessary and sufficient for photic entrainment to standard laboratory light/dark cycles. An obligatory role for the IGL–GHT in photic entrainment has not been demonstrated. Here we show that the IGL is necessary for entrainment of circadian rhythms to a skeleton photoperiod (SPP), an ecologically relevant lighting schedule congruous with light sampling behavior in nocturnal rodents. Rats with bilateral electrolytic IGL lesions entrained normally to lighting cycles consisting of 12 hr of light followed by 12 hr of darkness, but exhibited free-running rhythms when housed under an SPP consisting of two 1 hr light pulses given at times corresponding to dusk and dawn. Despite IGL lesions and other damage to the visual system, the SCN displayed normal sensitivity to the entraining light, as assessed by light-induced Fos immunoreactivity. In addition, all IGL-lesioned, free-running rats showed masking of the body temperature rhythm during the SPP light pulses. These results show that the integrity of the IGL is necessary for entrainment of circadian rhythms to a lighting schedule like that experienced by nocturnal rodents in the natural environment.

[1]  D. Asdourian,et al.  Entrainment of the rat's activity rhythm by cyclic light following lateral geniculate nucleus lesions , 1975, Physiology & Behavior.

[2]  C. Nemeroff,et al.  Neurotoxic amino acids and structurally related analogs. , 1977, Pharmacological reviews.

[3]  Z. Boulos,et al.  Circadian feeding and drinking rhythms in the rat under complete and skeleton photoperiods , 1983, Physiology & Behavior.

[4]  F. Stephan.  Circadian rhythms in the rat: Constant darkness, entrainment to T cycles and to skeleton photoperiods , 1983, Physiology & Behavior.

[5]  R. Moore.  Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. , 1983, Federation proceedings.

[6]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[7]  C. Ferris,et al.  Neuropeptide Y: Role in light-dark cycle entrainment of hamster circadian rhythms , 1984, Neuroscience Letters.

[8]  G. E. Pickard.  Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suppachiasmatic nucleus and the intergeniculate leaflet of the thalamus , 1985, Neuroscience Letters.

[9]  M. Harrington,et al.  Lesions of the Thalamic Intergeniculate Leaflet Alter Hamster Circadian Rhythms , 1986, Journal of biological rhythms.

[10]  G. E. Pickard,et al.  The Intergeniculate Leaflet Partially Mediates Effects of Light on Circadian Rhythms , 1987, Journal of biological rhythms.

[11]  L W Swanson,et al.  Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat , 1987, The Journal of comparative neurology.

[12]  R. F. Johnson,et al.  Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract , 1988, Brain Research.

[13]  P. Sawchenko,et al.  Detection of fos protein during osteogenesis by monoclonal antibodies , 1988, Molecular and cellular biology.

[14]  M. Harrington,et al.  Ablation of the geniculo-hypothalamic tract alters circadian activity rhythms of hamsters housed under constant light , 1988, Physiology & Behavior.

[15]  M. A. Rea.  Light increases Fos-related protein immunoreactivity in the rat suprachiasmatic nuclei , 1989, Brain Research Bulletin.

[16]  J. Meijer,et al.  Hamster circadian rhythms are phase-shifted by electrical stimulation of the geniculo-hypothalamic tract , 1989, Brain Research.

[17]  G. E. Pickard.  Entrainment of the circadian rhythm of wheel-running activity is phase shifted by ablation of the intergeniculate leaflet , 1989, Brain Research.

[18]  R. F. Johnson,et al.  Lateral geniculate lesions alter circadian activity rhythms in the hamster , 1989, Brain Research Bulletin.

[19]  F. Sharp,et al.  Light regulates expression of a Fos-related protein in rat suprachiasmatic nuclei. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[20]  W. Wisden,et al.  Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. , 1990, Science.

[21]  L. P. Morin,et al.  Photoperiodic responsiveness of hamsters with lesions of the lateral geniculate nucleus is related to hippocampal damage , 1990, Brain Research Bulletin.

[22]  J. Kornhauser,et al.  Photic and circadian regulation of c-fos gene expression in the hamster suprachiasmatic nucleus , 1990, Neuron.

[23]  M. Harrington,et al.  Geniculo-hypothalamic tract lesions block chlordiazepoxide-induced phase advances in Syrian hamsters , 1991, Brain Research.

[24]  K. Shinohara,et al.  Processing of photic information within the intergeniculate leaflet of the lateral geniculate body: Assessed by neuropeptide Y immunoreactivity in the suprachiasmatic nucleus of rats , 1993, Neuroscience.

[25]  M. Harrington,et al.  A phase-response curve to the benzodiazepine chlordiazepoxide and the effect of geniculo-hypothalamic tract ablation , 1993, Physiology & Behavior.

[26]  J. Money,et al.  Suprachiasmatic nucleus: the mind's clock , 1993 .

[27]  R. Moore,et al.  Intergeniculate leaflet: An anatomically and functionally distinct subdivision of the lateral geniculate complex , 1994, The Journal of comparative neurology.

[28]  N. Mrosovsky,et al.  Intergeniculate leaflet lesions and behaviorally-induced shifts of circadian rhythms , 1994, Brain Research.

[29]  F. Turek,et al.  Lesions of the thalamic intergeniculate leafleet block activity-induced phase shifts in the circadian activity rhythm of the golden hamster , 1994, Brain Research.

[30]  N. Mrosovsky.  In praise of masking: behavioural responses of retinally degenerate mice to dim light. , 1994, Chronobiology international.

[31]  G. E. Pickard.  Intergeniculate leaflet ablation alters circadian rhythms in the mouse , 1994, Neuroreport.

[32]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[33]  W. Schwartz,et al.  Temporal regulation of light-induced fos and fos-like protein expression in the ventrolateral subdivision of the rat suprachiasmatic nucleus , 1994, Neuroscience.

[34]  L. P. Morin.  The circadian visual system , 1994, Brain Research Reviews.

[35]  K. Schlingensiepen,et al.  Block of c‐Fos and JunB Expression by Antisense Oligonucleotides Inhibits Light‐induced‐Phase Shifts of the Mammalian Circadian Clock , 1995, The European journal of neuroscience.

[36]  D. Chadwick,et al.  Circadian clocks and their adjustment , 1995 .

[37]  N. Mrosovsky.  A non-photic gateway to the circadian clock of hamsters. , 1995, Ciba Foundation symposium.

[38]  K. Edelstein,et al.  Constant light induces persistent Fos expression in rat intergeniculate leaflet , 1996, Brain Research.

[39]  H. Eichenbaum.  Is the rodent hippocampus just for ‘place’? , 1996, Current Opinion in Neurobiology.

[40]  A. N. van den Pol,et al.  Neuropeptide Y-Mediated Long-Term Depression of Excitatory Activity in Suprachiasmatic Nucleus Neurons , 1996, The Journal of Neuroscience.

[41]  N. Mrosovsky.  LOCOMOTOR ACTIVITY AND NON‐PHOTIC INFLUENCES ON CIRCADIAN CLOCKS , 1996, Biological reviews of the Cambridge Philosophical Society.

[42]  E. Maywood,et al.  A Thalamic Contribution to Arousal‐induced, Non‐photic Entrainment of the Circadian Clock of the Syrian Hamster , 1997, The European journal of neuroscience.

[43]  R. Mistlberger,et al.  Scheduled activity reorganizes circadian phase of Syrian hamsters under full and skeleton photoperiods , 1997, Behavioural Brain Research.

[44]  N. Watson,et al.  Both Neuropeptide Y and Serotonin Are Necessary for Entrainment of Circadian Rhythms in Mice by Daily Treadmill Running Schedules , 1997, The Journal of Neuroscience.

[45]  T Roenneberg,et al.  Twilight Times: Light and the Circadian System , 1997, Photochemistry and photobiology.

[46]  M. Harrington.  The Ventral Lateral Geniculate Nucleus and the Intergeniculate Leaflet: Interrelated Structures in the Visual and Circadian Systems , 1997, Neuroscience & Biobehavioral Reviews.

[47]  The intergeniculate leaflet is necessary for entrainment to a skeleton photoperiod , 1997 .

[48]  M. A. Rea,et al.  Neuropeptide Y blocks light-induced phase advances but not delays of the circadian activity rhythm in hamsters , 1997, Neuroscience Letters.

[49]  M. Harrington,et al.  Neuropeptide Y and glutamate block each other's phase shifts in the suprachiasmatic nucleus in vitro , 1997, Neuroscience.

[50]  A. N. van den Pol,et al.  Phase Shifting of Circadian Rhythms and Depression of Neuronal Activity in the Rat Suprachiasmatic Nucleus by Neuropeptide Y: Mediation by Different Receptor Subtypes , 1998, The Journal of Neuroscience.

[51]  The intergeniculate leaflet does not mediate the disruptive effects of constant light on circadian rhythms in the rat , 1999, Neuroscience.