Leonard Kass

MIGRATION OF LIMULUS FOR MATING: RELATION TO LUNAR PHASE, TIDE HEIGHT, AND SUNLIGHT

In the spring, horseshoe crabs (Limulus polyphemus) along the eastern coast of North America migrate toward shore to build nests close to the waters edge. In 1984 the mating season near Woods Hole, Massachusetts, extended from 14 May to 7 July. Mating activity during this period fluctuated with the phase of the moon, the height of the tide, and diurnal changes in daylight. As the moon approached new and full phases, large numbers of animals migrated into the intertidal zone to mate and build nests. They appeared 1-2 h before high tide, and returned to deep water about 2 h after high tide. No mating activity occurred during low tides. The two daily high tides in this region are unequal in height. The inequality is greatest during new and full moons. At these times most animals migrated toward shore on the higher tide, which occurred in the late afternoon and throughout the night. As the moon passed through quadrature the tidal inequality diminished and reversed. Mating activity changed accordingly: shore ...

Efferent neurotransmission of circadian rhythms inLimulus lateral eye

SummaryWe investigated efferent neurotransmission in theLimulus lateral eye by studying the action of pharmacological agents on responses of photoreceptor cells in vitro. We recorded transmembrane potentials from single cells in slices of retina that were excised during the day and maintained for several days in a culture medium. Potentials recorded in the absence of pharmacological agents resemble those recorded from cells in vivo during the day.Octopamine, a putative efferent neurotransmitter, induced changes in photoreceptor potentials that mimicked in part those generated at night by a circadian clock located in the brain. Specifically, octopamine (100 to 500 μM) decreased the frequency of occurrence of quantum bumps in the dark and increased the amplitude of photoreceptor responses to intermediate and high light intensities. Similar actions were produced by naphazoline (25 to 100 (μM, potent agonist of octopamine), forskolin (8 to 400 μM, activator of adenylate cyclase), IBMX (1 mM, inhibitor of phosphodiesterase), and 8-bromo-cAMP (500 μM, analogue of cAMP). 8-bromo-cGMP (500 μM, analogue of cGMP) decreased the rate of spontaneous quantum bumps only.Our results support the hypothesis that (1) octopamine is an efferent neurotransmitter of circadian rhythms in theLimulus eye and that (2) it activates adenylate cyclase to increase levels of the second messenger, cAMP, in photoreceptor cells. Circadian changes in photoreceptor responses to moderate intensities may be a specific action of cAMP, since cGMP has no effect. Circadian changes in the rate of spontaneous quantum bumps may involve a less specific intermediate, since both cAMP and cGMP reduce bump rate. Characteristics of the retinal slice preparation precluded a detailed study of the effects of pharmacological agents on retinal morphology.

The morphology of the dorsal eye of the hydrothermal vent shrimp, Rimicaris exoculata

The bresiliid shrimp, Rimicaris exoculata, lives in large masses on the sides of hydrothermal vent chimneys at two sites on the Mid-Atlantic Ridge. Although essentially no daylight penetrates to depths of 3500 m, very dim light is emitted from the hydrothermal vents themselves. To exploit this light, R. exoculata has evolved a modified compound eye on its dorsal surface that occupies about 0.5% of the animals body volume. The eyes morphology suggests that it is extremely sensitive to light. The cornea of the dorsal eye is smooth with no dioptric apparatus. The retina consists of two wing-shaped lobes that are fused across the midline anteriorly. The rhabdomeral segments of the 7000 ommatidia form a compact layer of photosensitive membrane with an entrance aperture of more than 26 mm2. Within this layer, the volume density of rhabdom is more than 70%. Below the rhabdomeral segments, a thick layer of white diffusing cells scatters light upward into the photoreceptors. The arhabdomeral segments of the five to seven photoreceptors of each ommatidium are mere strands of cytoplasm that expand to accommodate the photoreceptor nuclei. The rhabdom is comprised of well-organized arrays of microvilli, each with a cytoskeletal core. The rhabdomeral segment cytoplasm contains mitochondria, but little else. The perikaryon contains a band of mitochondria, but has only small amounts of endoplasmic reticulum. There is no ultrastructural indication of photosensitive membrane cycling in these photoreceptors. Vestigial screening pigment cells and screening pigment granules within the photoreceptors are both restricted to the inner surface of the layer of the white diffusing cells. Below the retina, photoreceptor axons converge in a fanshaped array to enter the dorsal surface of the brain. The eyes size and structure are consistent with a role for vision in shrimp living at abyssal hydrothermal vents.

Circadian change in function of Limulus ventral photoreceptors

Efferent fibers from a central circadian clock innervate photoreceptors along the ventral nerve of Limulus and release octopamine when active. We have recorded ERG-like responses from the ventral eye in vivo over several day periods. We have also used intracellular microelectrodes to study changes in ventral photoreceptor function during exogenous applications of octopamine (the putative efferent neurotransmitter), IBMX (a phosphodiesterase inhibitor), and forskolin (an adenylate cyclase activator): (1) Responses to light measured at night from ventral photoreceptors in vivo are greater in amplitude than those recorded during the day; (2) Octopamine and agents that increase intracellular levels of cAMP in ventral photoreceptors decrease the rate of spontaneous (dark) bumps, increase photoreceptor response to light without changing threshold, and often increase the bump duration; and (3) These changes in function of ventral photoreceptors are similar to those that have been observed in the photoreceptor of the lateral eye during circadian clock activity at night, and in vitro in the presence of those same pharmacological agents.

Visual performance of horseshoe crabs day and night

A circadian clock modulates the structure and function of the lateral eyes of Limulus polyphemus, greatly increasing their sensitivity at night. During the mating season, male Limulus are visually attracted both day and night to females and objects that resemble females. This paper asks how well Limulus can see day and night, and whether the circadian changes in retinal sensitivity might influence the ability of these animals to find mates. We recorded the visual behavior of male and female horseshoe crabs in the vicinity of an object--a cement hemisphere (29.5 cm diameter) similar in size and shape to a female horseshoe crab--placed in a mating area near Mashnee Dike, Bourne, Massachusetts. Males oriented toward this target from an average distance of 0.94 m during the day and 0.88 m at night; and females appeared to avoid the target. We conclude that males can see potential mates at night almost as well as they can during the day. Apparently the circadian changes in the retina help compensate for the daily changes in illumination in the animals normal environment. This study provides the first evidence for a role of visual circadian rhythms in an animals natural behavior.

A circadian clock in the Limulus brain transmits synchronous efferent signals to all eyes

A circadian clock in the brain of the horseshoe crab, Limulus polyphemus, has an important role in the function of the peripheral visual system. At night, the clock transmits neural activity to the lateral, ventral, and median eyes via efferent optic nerve fibers. The activity occurs in synchronous bursts (maximum rate of 2 bursts/s) with individual efferent fibers contributing a single spike in each burst. The circadian efferent activity originates in the protocerebrum. Lateral connections synchronize the efferent activity recorded from the two halves of the protocerebrum, suggesting the existence of bilateral circadian oscillators. Circadian efferent activity survives excision of the brain and isolation of the protocerebrum. We conclude that circadian clock and its complex neural circuitry are fundamental components of the Limulus visual system.

Identification and Function of Octopamine and Tyramine Conjugates in the Limulus Visual System

Abstract: Major metabolites of octopamine and tyramine in the Limulus nervous system are identified here as γ‐glutamyl octopamine and γ‐glutamyl tyramine. We show that these conjugates are normal products of amine metabolism in Limulus, and that they are normally present in octopamine‐rich Limulus tissues. The synthesis of these conjugates is not restricted to nervous tissue, but the highest activity of γ‐glutamyl amine synthetase was measured in the CNS. Our interest in these molecules stems from our previous observations which showed that they were synthesized and stored in, and released from, the efferent fibers to Limulus eyes which modulate the sensitivity of the eyes to light. Here we provide direct evidence for the release of the conjugates from Limulus eyes in response to depolarization, and that γ‐glutamyl octopamine can increase the sensitivity of the lateral eye to light. Our observations lend support to the hypothesis that γ‐glutamyl octopamine may serve as an intercellular messenger in the Limulus visual system.

Retinal Anatomy of a New Species of Bresiliid Shrimp From a Hydrothermal Vent Field on the Mid-Atlantic Ridge

A new species of shrimp (Rimicaris sp.) was recently collected from the Snake Pit hydrothermal vent field on the Mid-Atlantic Ridge. Until the discovery in 1989 that the deep-sea, hydrothermal vent species, Rimicaris exoculata, possessed a hypertrophied dorsal eye, everyone believed that animals recovered from vent environments were blind. Like R. exoculata, Rimicaris sp., a small orange bresiliid shrimp, has an enlarged dorsal eye specialized for detecting light in a very dim environment instead of the expected compound eye. The individual lenses characteristic of a compound eye adapted for imaging have been replaced in Rimicaris sp. by a smooth cornea underlain by a massive array of photosensitive membrane. The number of ommatidia in this species is about the same as in shrimp species that live at the surface; however, the photoreceptors are larger in the deep-sea species and the shape of the photoreceptors is markedly different. The light-sensitive region of the photoreceptor is much larger than those of other shrimp and the rest of the receptor is much smaller than normal. All screening pigment has moved out of the path of incident light to a position below the retina, and the reflecting pigment cells have adapted to form a bright white diffusing screen between and behind the photoreceptors. The ultrastructure of the microvillar array comprising the rhabdom is typical for decapod crustaceans; however, there is a much greater volume density of rhabdom (80% to 85%) than normal. There is no ultrastructural evidence for cyclic rhabdom shedding or renewal. Rimicaris sp. has apparently adapted its visual system to detect the very dim light emitted from the throats of the black smoker chimneys around which it lives.

The eccentric cell of theLimulus lateral eye: encoder of circadian changes in visual responses

SummaryEfferent fibers from a central circadian clock innervate both photoreceptor cells and second-order neurons (eccentric cells) in the lateral compound eye ofLimulus, and release octopamine when activated. We have used intracellular microelectrodes to study the modulation of eccentric cell function by efferent optic-nerve activity, octopamine agonists, and a K+-channel blocker, TEA.1.The dramatic increase in response to light observed in the eccentric cell during efferent activity originates in the photoreceptor cell; efferent activity causes only small changes in the encoding of photoreceptor responses as nerve impulses by the eccentric cell. In contrast, octopamine agonists and TEA produce large changes in the impulse encoder of the eccentric cell.2.When lateral eyes are maintained in the dark, the rate of spontaneous impulse firing of eccentric cells increases in the presence of octopamine agonists, while spontaneous bump activity decreases. In contrast, endogenous efferent activity decreases both impulse rate and bump activity in the dark.3.TEA reduces the effects of lateral inhibition between neighboring eccentric cells.4.We suggest that the mechanisms for lateral inhibition and impulse generation are mediated by K+-channels that can be modulated by octopamine agonists. The distribution of efferent nerve terminals on the eccentric cells is such, however, that efferent optic-nerve activity can alter lateral inhibition, but is unlikely to produce large changes in the impulse encoder.

Circadian Rhythms in Retinal Function

The retina encodes and transmits information to the brain about the photic environment. In a number of animals the brain feeds back to the retina signals that modify the configuration of ganglion-cell receptive fields (Miles, 1970; Pearlman & Hughes, 1976), adapt the retina to changes in ambient illumination (Arechiga & Wiersma, 1969; Barlow et al, 1977; Fleissner & Fleissner, 1978; Levinson & Burnside, 1981; Yamashita & Tateda, 1981), or control metabolic processes in the retina (Chamberlain & Barlow, 1979; Teirstein et al, 1980). The efferent control of retinal function may be mediated by neural pathways or by circulating neurohormones.