Summary
We have used chronic, or long-term, intracellular recording combined with simultaneous extracellular recording of optic nerve activity to examine the neurophysiological basis of circadian rhythmicity in theBulla eye. We report that:
-
1.
Continuous intracellular recordings from R-type photoreceptors were maintained for up to 28 h. These recordings reveal that in constant conditions R-type cells do not exhibit rhythms in membrane potential which correlate with the circadian rhythm in compound action potential frequency expressed by the eye.
-
2.
Continuous intracellular recordings from basal retinal neurons were maintained for up to 74 h. These recordings reveal that in constant conditions basal retinal neurons exhibit clear circadian rhythms in membrane potential and action potential frequency which are synchronized with the circadian rhythm in compound action potential frequency. Action potentials in individual basal retinal neurons correlate one-for-one with the compound action potentials in the optic nerve over the entire circadian cycle. The basal retinal neurons depolarize during the active phase of the compound action potential rhythm (projected day), relative to their membrane potential during the inactive phase of the rhythm (projected night).
-
3.
The phase relationship between the rhythm in basal retinal neuron membrane potential and action potential frequency is such that the rise in membrane potential from its most hyperpolarized point precedes, or is synchronous with, the increase in action potential frequency observed near projected dawn. This suggests that the membrane potential rhythm drives the circadian rhythm in impulse frequency.
-
4.
The quantitative relationship between basal retinal neuron membrane potential and action potential frequency is not linear, and varies predictably with circadian phase. Following the interval of peak impulse frequency the rate of impulse production declines more rapidly than does the membrane potential. Also, the impulse frequency at a given membrane potential is lower during the falling phase of the circadian cycle than during the rising phase.
-
5.
In conclusion, we find that the basal retinal neurons are at minimum a pacemaker output pathway, and are likely the circadian pacemaker itself. We find no role for the R-type photoreceptor in the generation of circadian rhythmicity by theBulla eye.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- BRN :
-
basal retinal neuron
References
Block G, Friesen W (1981) Electrophysiology ofBulla eyes: cirrcadian rhythm and intracellular responses to illumination. Neurosci Abstr 7:45
Block GD, McMahon DG (1983) Localized illumination of theAplysia andBulla eye reveals new relationships between retinal layers. Brain Res 265:134–137
Block GD, McMahon DG (1984) Cellular analysis of theBulla ocular circadian pacemaker system. III. Localization of the circadian pacemaker system. J Comp Physiol A 155:387–395
Block GD, Roberts MH (1981) Circadian pacemaker in theBursatella eye: properties of the rhythm and its effect on locomotor behavior. J Comp Physiol 142:403–410
Block GD, Wallace SF (1982) Localization of a circadian pacemaker in the eye of a mollusc,Bulla. Science 217:155–157
Block GD, McMahon DG, Wallace SF, Friesen WO (1984) Cellular analysis of theBulla ocular circadian pacemaker system. I. A model for retinal organization. J Comp Physiol A 155:365–378
Corrent G, Eskin A, Kay I (1982) Entrainment of the circadian rhythm from the eye ofAplysia: Role of serotonin. Am J Physiol: R333–R338
Eskin A (1977) Neurophysiological mechanisms involved in photoentrainment of the circadian rhythm from theAplysia eye. J Neurobiol 8:273–299
Eskin A (1982) Increasing external K+ blocks phase shifts in a circadian rhythm produced by serotonin or 8-benzylthiocAMP. J Neurobiol 13:241–249
Eskin A, Harcombe E (1977) Eye ofNavanax: optic activity, circadian rhythm and morphology. Comp Biochem Physiol 57A:443–449
Jacklet JW (1969) Circadian rhythm of optic nerve impulses recorded in darkness from the isolated eye ofAplysia. Science 164:562–563
Jacklet JW, Colquhoun W (1983) Ultrastructure of photoreceptors and circadian pacemaker neurons in the eye of a gastropod,Bulla. J Neurocytol 12:673–696
McMahon DG, Block GD (1982) Organized photoreceptor layer is not required for light response in three opisthobranch eyes. Neurosci Abstr 8:33
McMahon DG, Block GD (1983) Long-term intracellular recording from lower retinal neurons in theBulla eye: rhythms in membrane potential and impulse frequency follow circadian rhythm. Neurosci Abstr 9:623
Strumwasser F, Viele DP, Scotese JM (1979) Dissection of a neuronal circadian oscillator system in the eye ofAplysia: Intracellular recording from single disconnected photoreceptors in cell culture. Neurosci Abstr 5:809
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
McMahon, D.G., Wallace, S.F. & Block, G.D. Cellular analysis of theBulla ocular circadian pacemaker system. J. Comp. Physiol. 155, 379–385 (1984). https://doi.org/10.1007/BF00610591
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00610591