BRAIN PHOTORECEPTOR PATHWAYS CONTRIBUTING TO CIRCADIAN RHYTHMICITY IN CRAYFISH

Freshwater crayfish have three known photoreceptive systems: the compound eyes, extraretinal brain photoreceptors, and caudal photoreceptors. The primary goal of the work described here was to explore the contribution of the brain photoreceptors to circadian locomotory activity and define some of the underlying neural pathways. Immunocytochemical studies of the brain photoreceptors in the parastacid (southern hemisphere) crayfish Cherax destructor reveal their expression of the blue light-sensitive photopigment cryptochrome and the neurotransmitter histamine. The brain photoreceptors project to two small protocerebral neuropils, the brain photoreceptor neuropils (BPNs), where they terminate among fibers expressing the neuropeptide pigment-dispersing hormone (PDH), a signaling molecule in arthropod circadian systems. Comparable pathways are also described in the astacid (northern hemisphere) crayfish Procambarus clarkii. Despite exhibiting markedly different diurnal locomotor activity rhythms, removal of the compound eyes and caudal photoreceptors in both C. destructor and P. clarkii (leaving the brain photoreceptors intact) does not abolish the normal light/dark activity cycle in either species, nor prevent the entrainment of their activity cycles to phase shifts of the light/dark period. These results suggest, therefore, that crayfish brain photoreceptors are sufficient for the entrainment of locomotor activity rhythms to photic stimuli, and that they can act in the absence of the compound eyes and caudal photoreceptors. We also demonstrate that the intensity of PDH expression in the BPNs varies in phase with the locomotor activity rhythm of both crayfish species. Together, these findings suggest that the brain photoreceptor cells can function as extraretinal circadian photoreceptors and that the BPN represents part of an entrainment pathway synchronizing locomotor activity to environmental light/dark cycles, and implicating the neuropeptide PDH in these functions. (Author correspondence: bbeltz@wellesley.edu)     

Circadian organization in the pigeon,Columba livia: the role of the pineal organ and the eye

Summary The roles of the pineal organ and the eye in the control of circadian locomotor rhythmicity were studied in the pigeon (Columba livia). Neither pinealectomy nor blinding abolished the circadian rhythms in constant dim light conditions (LLdim). All the pinealectomized birds and the blinded birds entrained to light-dark (LD) cycles with no discernible anticipatory activity. However, the birds which had been both pinealectomized and blinded showed no circadian rhythms in prolonged LLdim. These birds entrained to LD cycles with anticipatory activity and showed residual rhythmicity for a while after transfer from LD cycles to LLdim. Continuous administration of melatonin induced suppression of the circadian rhythms and reduced total amount of locomotor activity in LLdim. These results suggest that not only the pineal organ but also the eye (perhaps the retina) is involved in the pigeon's circadian system.Abbreviations NAT N-acetyltransferase - LLdim constant dim light - cadian period - SCN suprachiasmatic nucleus - circadian activity time - LD light-dark     

Pineal and retinal melatonin is involved in the control of circadian locomotor activity and body temperature rhythms in the pigeon

Summary Although pinealectomy or blinding resulted in loss of the clarity of the free-running rhythm of locomotor activity and body temperature and reduced the peak level of circulating melatonin rhythms to approximately a half in intact pigeons, neither pinealectomy nor blinding abolished any of these rhythms. However, when pinealectomy and blinding were combined, the rhythms of locomotor activity and body temperature disappeared in prolonged constant dim light, and melatonin concentration was reduced to the minimum level of detection. In order to examine the role of melatonin in the pigeon's circadian system, it was administered either daily or continuously to PX + EX-pigeons in LLdim. Daily administration of melatonin restored circadian rhythms of locomotor activity which entrained to melatonin injections, but continuous administration did not induce any remarkable change of locomotor activity. These results suggest that melatonin synthesized in the pineal body and the eye contributes to circulating melatonin and its rhythmicity is important for the control of circadian rhythms of locomotor activity and body temperature in the pigeon.Abbreviations LD Light-dark - LLdim constant dim light - LLbright constant bright light - PX pinealectomy - EX blinding - SCN suprachiasmatic nucleus     

Sustaining fibers in the rock lobster

The properties of sustaining fibers (SuF's), whose firing frequency is related to the ambient light intensity, were studied in the rock lobster. Most of the firing patterns shown under various conditions were demonstrated to be physiological, by using chronic implantation techniques. Unusual activity at high light intensities suggests that the lobster visual system is equipped to function only under dim light conditions. Unlike the crayfish, the lobster SuF's do not always indicate light levels but only changes in light intensity. It is suggested that the input from these fibers has a large influence on locomotor activity.     

Synaptic transmission in the pineal eye of young Xenopus laevis tadpoles: a role for NMDA and non-NMDA glutamate and non-glutaminergic receptors?

The pineal eye of Xenopus laevis tadpoles is directly photosensitive. A sudden reduction in light intensity produces a burst of activity in the pineal ganglion cells, which is closely followed by the onset of swimming. In this paper I present the results of experiments on the effects of agonists and antagonists of candidate pineal transmitters on ganglion cell activity. I found that NMDA and non-NMDA excitatory amino acid (EAA) agonists increased pineal activity, indicating the presence of both types of receptor. Kynurenic acid reduced activity, thus confirming that the photoreceptor transmitter is an EAA. Under physiological conditions, CNQX blocked activity almost completely whilst AP5 had little effect. In Mg²⁺-free saline CNQX had a considerably smaller effect, but joint application of CNQX and AP5 blocked almost all activity; therefore, the NMDA receptors are subject to blockage by Mg²⁺. Although GABA_A and ACh receptors appear to be present, no evidence was found for GABA or ACh as pineal transmitters. In addition, 5-HT had no effect on pineal activity. The main pineal transmitter is an EAA acting on ganglion cells through both NMDA and non-NMDA receptors. Other receptors are present but appear to have no role in controlling pineal activity at this stage. Accepted: 1 March 1997     

Nonvisual photoreceptors of the deep brain, pineal organs and retina

The role of the nonvisual photoreception is to synchronise periodic functions of living organisms to the environmental light periods in order to help survival of various species in different biotopes. In vertebrates, the so-called deep brain (septal and hypothalamic) photoreceptors, the pineal organs (pineal- and parapineal organs, frontal- and parietal eye) and the retina (of the "lateral" eye) are involved in the light-based entrain of endogenous circadian clocks present in various organs. In humans, photoperiodicity was studied in connection with sleep disturbances in shift work, seasonal depression, and in jet-lag of transmeridional travellers. In the present review, experimental and molecular aspects are discussed, focusing on the histological and histochemical basis of the function of nonvisual photoreceptors. We also offer a view about functional changes of these photoreceptors during pre- and postnatal development as well as about its possible evolution. Our scope in some points is different from the generally accepted views on the nonvisual photoreceptive systems. The deep brain photoreceptors are hypothalamic and septal nuclei of the periventricular cerebrospinal fluid (CSF)-contacting neuronal system. Already present in the lancelet and representing the most ancient type of vertebrate nerve cells ("protoneurons"), CSF-contacting neurons are sensory-type cells sitting in the wall of the brain ventricles that send a ciliated dendritic process into the CSF. Various opsins and other members of the phototransduction cascade have been demonstrated in telencephalic and hypothalamic groups of these neurons. In all species examined so far, deep brain photoreceptors play a role in the circadian and circannual regulation of periodic functions. Mainly called pineal "glands" in the last decades, the pineal organs actually represent a differentiated form of encephalic photoreceptors. Supposed to be intra- and extracranially outgrown groups of deep brain photoreceptors, pineal organs also contain neurons and glial elements. Extracranial pineal organs of submammalians are cone-dominated photoreceptors sensitive to different wavelengths of light, while intracranial pineal organs predominantly contain rod-like photoreceptor cells and thus scotopic light receptors. Vitamin B-based light-sensitive cryptochromes localized immunocytochemically in some pineal cells may take part in both the photoreception and the pacemaker function of the pineal organ. In spite of expressing phototransduction cascade molecules and forming outer segment-like cilia in some species, the mammalian pineal is considered by most of the authors as a light-insensitive organ. Expression of phototransduction cascade molecules, predominantly in young animals, is a photoreceptor-like characteristic of pinealocytes in higher vertebrates that may contribute to a light-percepting task in the perinatal entrainment of rhythmic functions. In adult mammals, adrenergic nerves--mediating daily fluctuation of sympathetic activity rather than retinal light information as generally supposed--may sustain circadian periodicity already entrained by light perinatally. Altogether three phases were supposed to exist in pineal entrainment of internal pacemakers: an embryological synchronization by light and in viviparous vertebrates by maternal effects (1); a light-based, postnatal entrainment (2); and in adults, a maintenance of periodicity by daily sympathetic rhythm of the hypothalamus. In addition to its visual function, the lateral eye retina performs a nonvisual task. Nonvisual retinal light perception primarily entrains genetically-determined periodicity, such as rod-cone dominance, EEG rhythms or retinomotor movements. It also influences the suprachiasmatic nucleus, the primary pacemaker of the brain. As neither rods nor cones seem to represent the nonvisual retinal photoreceptors, the presence of additional photoreceptors has been supposed. Cryptochrome 1, a photosensitive molecule identified in retinal nerve cells and in a subpopulation of retinal photoreceptors, is a good candidate for the nonvisual photoreceptor molecule as well as for a member of pacemaker molecules in the retina. When comparing various visual and nonvisual photoreceptors, transitory, "semi visual" (directional) light-perceptive cells can be detected among them, such as those in the parietal eye of reptiles. Measuring diffuse light intensity of the environment, semivisual photoreceptors also possess some directional light perceptive capacity aided by complementary lens-like structures, and screening pigment cells. Semivisual photoreception in aquatic animals may serve for identifying environmental areas of suitable illumination, or in poikilotermic terrestrial species for measuring direct solar irradiation for thermoregulation. As directional photoreceptors were identified among nonvisual light perceptive cells in the lancelet, but eyes are lacking, an early appearance of semivisual function, prior to a visual one (nonvisual --> semivisual --> visual?) in the vertebrate evolution was supposed.     

Photosensory input pathways in the medicinal leech

Summary The medicinal leech,Hirudo medicinalis possesses two types of photosensory organs: five bilateral pairs of eyes embedded in two longitudinal rows in the dorsal surface of the head, and seven bilateral pairs of sensilla situated in both the dorsal and the ventral surface of each of the 21 body segments. The photoreceptor cells of each eye or sensillum project their axons centrally via a characteristic cephalic or segmental nerve which carries the photosensory input to the brain or to the segmental ganglion. In response to a pulse of light the photoreceptors produce a train of impulses whose frequency first rises to anearly peak and then declines to asteady state plateau at which it remains until the end of the pulse. The amplitude of the early peak response and the level of the steady state plateau rise linearly with the log of the light pulse intensity, but the dynamic range of the early peak response is much narrower than that of the plateau. Both ocular and sensillar photoreceptors adapt to the intensity of interpulse background illumination; the ocular receptors adapt so completely that their level of background activity is nearly independent of the background light intensity, whereas the ventral sensillar photoreceptors adapt incompletely, so that their background activity rises with the background light intensity. Ocular and sensillar photoreceptors make their maximal response to green light at a wavelength of about 540 nm. They are almost insensitive to red and violet light at both extremes of the visible spectrum. The photosensory response of a single eye is directionally selective, whereas that of a single sensillum has much less directional selectivity. Several higher order sensory neurons were identified in the segmental ganglion that receive photosensory input from the sensilla. One of these neurons has the sensillum in the ipsilateral dorso-medial body wall of the same segment as its receptive field and another neuron the bilateral set of ventral sensilla in the body wall of the next posterior segment.We are indebted to Frank S. Werblin for valuable advice and discussions. We thank Kenneth L. Carlock for designing and constructing much of the special electronic equipment used in this study. We also thank Alexander Petruncola for his helpful suggestions regarding the computational analysis of the experimental results and for writing the computer programs used in the processing of the data.This research was supported by Grant No. GB 31933X from the National Science Foundation, and NIH research grant No. GM 17866 and Training Grant No. GM 00829 from the Institute for General Medical Sciences.     

Pigment migration and illumination of single photoreceptors in a moth

Summary The relation between intensity of illumination of single photoreceptors and position of the screening pigment was studied in the compound eye of the moth Deilephila elpenor. The amplitude of the response to test flashes of white light was measured in 7 dark adapted photoreceptor cells with the screening pigment in the extreme distal and in a proximal position. The experiments demonstrate that the response amplitude of individual photoreceptors varies with the pigment position. The associated variation in screening effect was 1.0 to 1.9 log units.The research reported in this study was supported by Swedish Medical Research Council, Sällskapet för Medicinsk Forskning and Stifteisen Gustaf och Tyra Svenssons Minne.     

Effect of light intensity on the locomotor activity rhythm of Talitrus saltator (Montagu 1808) from Korba Beach

In this work, we investigate the locomotor behaviour of Talitrus saltator (Montagu 1808) for a population collected from the supralittoral zone of Korba beach. The locomotor activity rhythm was recorded for adult individuals during 10 summer days under continuous light with four different luminous intensities: 5 lux (N = 30), 35 lux (N = 30), 75 lux (N = 30) and 140 lux (N = 15). By the end of the experiments, 100% of the considered individuals were found alive under light intensities of 35 and 140 lux, whereas only 86 and 90% were found alive under light intensity of 5 and 75 lux, respectively. Furthermore, whatever the imposed luminous intensity is, actograms showed a clear drift to the right lengthening day after day the circadian period. Moreover, we found that by raising the light intensity, the drift becomes increasingly important. Actograms as well as activity curves, results showed that the locomotor activity profiles are mainly unimodal and their percentage increases when increasing the light intensity. Furthermore, periodogram analysis highlighted the presence of ultradian and circadian components where the longest periods were observed with the highest luminous intensity. In addition, the locomotor activity rhythm was statistically more defined and individuals of Talitrus saltator were significantly more active under the lowest luminous intensity.     

The effects of pinealectomy and blinding on the circadian locomotor activity rhythm in the Japanese newt,Cynops pyrrhogaster

We examined the effects of pinealectomy and blinding (bilateral ocular enucleation) on the circadian locomotor activity rhythm in the Japanese newt, Cynops pyrrhogaster. The pinealectomized newts were entrained to a light-dark cycle of 12 h light and 12 h darkness. After transfer to constant darkness they showed residual rhythmicity for at least several days which was gradually disrupted in prolonged constant darkness. Blinded newts were also entrained to a 12 h light/12 h dark cycle. In subsequent constant darkness they showed free-running rhythms of locomotor activity. However, the freerunning periods noticeably increased compared with those observed in the previous period of constant darkness before blinding. In blinded newts entrained to the light/dark cycle the activity rhythms were gradually disrupted after pinealectomy even in the presence of the light/dark cycle. These results suggest that both the pineal and the eyes are involved in the newt's circadian system, and also suggest that the pineal of the newt acts as an extraretinal photoreceptor which mediates the entrainment of the locomotor activity rhythm.Abbreviations circadian period - DD constant darkness - LD cycle, light-dark cycle - LD 12:12 light-dark cycle of 12 h light and 12 h darkness     

FINE STRUCTURE OF THE PINEAL ORGANS OF THE ADULT FROG, RANA PIPIENS

Frontal organs and epiphyses of the pineal system from the adult frog, Rana pipiens, were fixed in s-collidine-buffered osmium tetroxide, embedded in Epon 812, and examined by electron microscopy. Epiphyseal material was also fixed in a variety of ways and subjected to a series of cytochemical tests for light microscopy. An ultrastructure resembling that of lateral eye retina is confirmed in this species. Photoreceptor cells of the epiphysis and frontal organ display many cytological features similar to those of retinal rods and cones in the arrangement of their outer and inner segments and synaptic components. However, in these pineal organs the outer segments are disoriented relative to each other and may display a disarranged internal organization unlike normal retinal photoreceptors. Furthermore, other pineal outer segments often appear degenerate. Since immature stages in the development of new outer segments also appear to be present, adult pineal photoreceptors are probably engaged in a constant renewal of outer segment membranes. The evidence further suggests that macrophages are involved in phagocytosis of degenerated outer segments. Postulated photoreceptor activities and the possibility of secondary pineal functions, such as secretion, are discussed in view of current morphological and cytochemical findings.     

A comparison of some photoreceptor characteristics in the pineal and retina

Summary Immunocytochemistry with a rod-specific antiserum was used to study the post-hatch development (2 days–300 days) of photoreceptor elements within the pineal of the Japanese quail. At all ages staining was restricted to limited numbers of pinealocytes scattered throughout the gland. An enzyme-linked immunosorbent assay (ELISA), with the same rod-specific antibody, was then used to obtain a quantitative measure of rod opsin in total eye and pineal extracts in both the developing retina and pineal. The opsin content of both tissues shows a marked increase during the first 30 days after hatch and then plateaued to 0.84±0.02 nmoles opsin in the eye and 2.20±0.11 pmoles opsin equivalents in the pineal. The increase in opsin in the retina may be associated with continued post-hatch development of the photoreceptors. We then attempted to demonstrate the presence of the rhodopsin chromophore within pineal and retinal extracts using HPLC analysis. In both retinal and pineal extracts, 11-cis retinaldehyde was identified and a light-induced shift from the 11-cis to the all-trans isomer was clearly shown. This analysis also allowed us to calculate the total content of 11-cis and all-trans retinaldehyde (derived from both rod and non-rod photoreceptors) of the eye and pineal (eye: 1.7±0.2 nmoles; pineal: 4.6±0.5 pmoles). In the quail eye, the total amount of retinaldehyde is more than twice the amount of rod-like opsin. This probably reflects the large contribution of cones in the quail retina; the cone pigments will contribute to the retinaldehyde content but are not recognized by the rodspecific antibodies. In the pineal, we also found more than double the concentration of retinaldehyde than we would have predicted from the amount of rod-like opsin. These results, coupled with our immunocytochemical findings, suggest that the quail pineal contains at least two classes of photoreceptor, some rod-like, others non rod-like.Abbreviations HPLC high-performance liquid chromatography - ELISA enzyme-linked immunosorbent assay Work conducted while member of the AFRC Research Group on Photoperiodism and Reproduction, Department of Zoology, University of Bristol, Bristol, BS8 1UG, United Kingdom     

Circadian Rhythms of Locomotor Activity in Lycosa tarentula (Araneae,Lycosidae) and the Pathways of Ocular Entrainment

Lycosa tarentula is a ground-living spider that inhabits a burrow where it awaits the appearance of prey or conspecifics. In this study, circadian rhythms of locomotor activity were examined as well as the ocular pathway of entrainment. Thirty-three adult virgin females were examined under constant darkness (DD); all of them exhibited robust circadian rhythms of locomotor activity with a period averaging 24.1h. Fourteen of these spiders were studied afterwards under an LD 12:12 cycle; they usually entrained to in the first or second day, even when the light intensity was as low as 1 lx. During the LD cycle, locomotor activity was generally restrained to the darkness phase, although several animals showed a small amount of diurnal activity. Ten males were also examined under LD; they were also nocturnal, but were much more active than the females. Seven females were examined under constant light (LL); under this they became arrhythmic. Except for the anterior median eyes (OMAs), all the eyes were capable of entraining the locomotor activity to an LD cycle. These results demonstrate that under laboratory conditions and low light intensities locomotor activity of Lycosa tarentula is circadian and in accordance with Aschoff's 'rule'. Only OMAs are unable to entrain the rhythm; the possible localization of circadian clock is therefore discussed.     

Kinetics in metabolic control of time measurement in photoperiodism

Abstract

The period length of the locomotor activity rhythm of Drosophila melanogaster wild form is under conditions of continuous weak red light 23.38 h, whereas die eye mutants Ly3 with a 23.71 h mean period and JK 84 with 23.14 h differ significantly. This might be due to a changed perception of light and not the result of a change in the circadian pacemaker by the mutation.

The mutant sine oculis exhibits a normal activity rhythm if the complex eyes are not completely reduced. If this is the case, the activity pattern is either less rhythmic, composed of several rhythms with different periods or truely arrhythmic depending on the individual fly.

Since the mutation in sine oculis affects in addition to the complex eye the distal part of die medulla and the lamina of the optic lobe, it is suggested that the circadian pacemakers for the locomotor activity rhythm is localized in these parts.     

Retinal and extraretinal photoreceptors mediate entrainment of the circadian locomotor rhythm in lizards

Summary The circadian locomotor activity rhythms of 7 species of lizards can readily be entrained (synchronized) toLD12: 12 (30–50 lux: 0) fluorescent light cycles after complete surgical removal of both eyes. Removal of the parietal eye and pineal organ does not prevent entrainment of blinded lizards. Appropriate control experiments established that lightper se, and not low amplitude temperature cycles or other obvious environmental variables, was the entraining stimulus for blinded lizards. In some cases, blocking the penetration of light to the brains of blinded lizards caused them to free-run (express their endogenous circadian rhythm) in the presence of a dim green light cycle, to which they had previously entrained, suggesting that the brain is the site of the extraretinal photoreceptor(s) mediating entrainment. The extraretinal photoreceptor(s) is capable of intensity discrimination since changing the intensity of aLD 12: 12 fluorescent light cycle caused a change in the phase-relationship between the entrained activity rhythm and the light cycle in a blinded gekko. The lateral eyes are also involved in mediating entrainment since removal of the lateral eyes of thoseSceloporus olivaceus which previously entrained to a dim green light cycle [LD 12: 12 (0.05 lux: 0)] caused them to free-run. Also, blinding had noticeable effects on the entrained activity patterns of some species of lizards.I thank Michael Menaker, Jeffrey Elliott, Sue Binkley, Joseph Silver, Ed Kluth, George Wyche, Bruee Rouse, Nancy Leshikar, Lili Mostafavi, Janet Alvis, Celeste Cromack, A. L. Mackey and Jean Rogers for their suggestions and technical assistance. Support for this work was provided by NIH grant HD-03803-02 (to M. Menaker); NSP grant GB-8138 (to M. Menaker); NSF traineeship GZ-1336 (to H. Underwood); and MH traineeship 5T01GM00836-09 (to H. Underwood).     

Immunocytochemical and electron-microscopic investigations of the pineal organ in adult agamid lizards,Uromastix hardwicki

Summary Lacertilian species display a remarkable diversity in the organization of the neural apparatus of their pineal organ (epiphysis cerebri). The occurrence of immunoreactive S-antigen and opsin was investigated in the retina and pineal organ of adult lizards, Uromastix hardwicki. In this species, numerous retinal photoreceptors displayed S-antigen-like immunoreactivity, whereas only very few pinealocytes were labeled. Immunoreactive opsin was found neither in retinal photoreceptors nor in pinealocytes. Electron microscopy showed that all pinealocytes of Uromastix hardwicki resemble modified pineal photoreceptors. A peculiar observation is the existence of a previously undescribed membrane system in the inner segments of these cells. It is evidently derived from the rough endoplasmic reticulum but consists of smooth membranes. The modified pineal photoreceptor cells of Uromastix hardwicki were never seen to establish synaptic contacts with somata or dendrites of intrapineal neurons, which are extremely rare. Vesiclecrowned ribbons are prominent in the basal processes of the receptor cells, facing the basal lamina or establishing receptor-receptor and receptor-interstitial type synaptoid contacts. Dense-core granules (60–250 nm in diameter) speak in favor of a secretory activity of the pinealocytes. Attention is drawn to the existence of receptor-receptor and receptor-interstitial cell contacts indicating intramural cellular relationships that deserve further study.Supported by the Deutsche Forschungsgemeinschaft (Ko 758/31) and the Deutscher Akademischer Austauschdienst (Senior DAAD Research Fellowship to M.A.H.)     

The effect of light adaptation on the dynamic properties of phototransduction in the fly,Phormia regina

The static and dynamic characteristics of phototransduction were studied in photoreceptors of the compound eye of the fly Phormia regina (Calliphoridae) using a green light emitting diode driven by a controlled current source. The LED provides sufficiently intense light to investigate the behaviour of the receptors over about half of the dark adapted range of the response versus log intensity curve. The effects of constant adapting light intensities upon the step response and upon the frequency response and coherence functions were examined. Using both methods the effect of light adaptation upon receptor sensitivity can be closely approximated by a similar linear dependence of log sensitivity upon log adapting intensity. However, there was no reliably detectable effect of light adaptation upon the time constant of the response over the range of adapting intensities used.Abbreviation LED Light Emitting Diode     

The role of dermal photoreceptors during the sea lamprey (<Emphasis Type="Italic">Petromyzon marinus</Emphasis>) spawning migration

Light avoidance in larval lampreys is mediated by dermal photoreceptors located in the tail. These photoreceptors continue to function in adults, but they seem redundant because post-metamorphic lampreys possess well-developed eyes. This study examined the role of dermal photoreceptors in adult sea lampreys by testing whether temperature-induced changes in refuge-seeking behavior are mediated by a reduction in dermal photosensitivity. In a lighted arena containing a single shaded refuge platform, lampreys at 22°C displayed five times less search activity and were less likely to attach beneath the refuge platform than lampreys at either 7 or 15°C. A behavioral assay for tail photosensitivity (locomotor response to tail illumination) revealed a corresponding reduction in dermal photosensitivity at 22°C. Moreover, the responses to head illumination (eyes and pineal) did not correspond with the observed light avoidance behaviors. The head was less responsive to light than the tail and was not influenced by temperature. These results provide strong evidence that the dermal photoreceptors continue to mediate light avoidance in adult lampreys, even though adults possess fully functional eyes. The fact that the eyes apparently do not take on this role suggests that there is functional specialization between these two light sensing systems.     

The circadian rhythm and photosensitivity of small impulses of the Bulla eye

Summary The eye of the mollusk Bulla gouldiana contains a pacemaker that generates a circadian rhythm in compound action potentials (CAPs) in the optic nerve. In this paper, we present evidence of a second circadian rhythm in the optic nerve of the eye maintained in darkness at 15 °C. This is a rhythm in the frequency of small (10–40 V) neural impulses that occurs about 12 h out-of-phase with the rhythm in CAPs. Typically, the small-spike frequency is at a minimum within an hour of the peak in CAP frequency and is maximal during the subjective night. Like the CAP rhythm, the phase of the small-spike rhythm is determined by the prior light/dark cycle. A rebound in small-spike activity following the end of a light pulse and the presence of photoinhibited impulses in surgically reduced eyes suggests that the cells that generate the small-spikes may be photoreceptors that are inhibited by light. In addition, by using isolated nervous system preparations, we have found that smallspikes occur in the two optic nerves in a one-for-one relationship immediately following a light-to-dark transition. This inter-eye communication may be involved in the coupling of the ocular pacemakers.Abbreviations ASW artificial sea water - BRN basal retinal neuron - CAP compound action potential