Histochemical localization of acetylcholinesterase in the lateral eye and brain of Limulus polyphemus: Might acetylcholine be a neurotransmitter for lateral inhibition in the lateral eye?

1994 ◽  
Vol 11 (5) ◽  
pp. 989-1001 ◽  
Author(s):  
Eric P. Hornstein ◽  
Daniel L. Sambursky ◽  
Steven C. Chamberlain

AbstractThe distribution of acetylcholinesterase (AChE) in the lateral eye and brain of the horseshoe crab was investigated with histochemical means using standard controls to eliminate butyrylcholinesterase and nonspecific staining. Intense staining was observed in the neural plexus of the lateral compound eye, in the lateral optic nerve, and in various neuropils of the brain. Nerve fibers with moderate to weak staining were widespread in the brain. No sornata were stained in either the lateral eye or the brain. The distribution of acetylcholinesterase in the supraesophageal ganglia and nerves of the giant barnacle was also investigated for comparison. Although both the median optic nerve of the barnacle and the lateral optic nerve of the horseshoe crab appear to contain the fibers of histaminergic neurons, only the lateral optic nerve of the horseshoe crab shows AChE staining. Other parts of the barnacle nervous system, however, showed intense AChE staining. These results along with the histochemical controls eliminate the possibility that some molecule found in histaminergic neurons accounted for the AChE staining but support the possibility that acetylcholine might be involved as a neurotransmitter in lateral inhibition in the horseshoe crab retina. Two reasonable neurotransmitter candidates for lateral inhibition, histamine and acetylcholine, must now be investigated.

Author(s):  
James A. Anderson

This chapter gives three examples of real neural computation. The conclusion is that the “brain doesn’t work by logic.” First, is the Limulus (horseshoe crab) lateral eye. The neural process of “lateral inhibition” tunes the neural response of the compound eye to allow crabs to better see other crabs for mating. Second, the retina of the frog contains cells that are selective to specific properties of the visual image. The frog responds strongly to the moving image of a bug with one class of selective retinal receptors. Third, experiments on patients undergoing neurosurgery for epilepsy found single neurons in several cortical areas that were highly selective to differing images, text strings, and spoken names of well-known people. In addition, new selective responses could be formed quickly. The connection to concepts in cognitive science seems inevitable. One possible mechanism is through associatively linked “cell assemblies.”


Author(s):  
Steven C. Chamberlain

The lateral eye of the horseshoe crab, Limulus polyphemus, is an important model system for studies of visual processes such as phototransduction, lateral inhibition, and light adaptation. It has also been the system of choice for pioneering studies of the role of circadian efferent input from the brain to the eye. For example, light and efferent input interact in controlling the daily shedding of photosensitive membrane and photomechanical movements. Most recently, modeling efforts have begun to relate anatomy, physiology and visually guided behavior using parallel computing. My laboratory has pursued collaborative morphological studies of the compound eye for the past 15 years. Some of this research has been correlated structure/function studies; the rest has been studies of basic morphology and morphological process.


1990 ◽  
Vol 95 (2) ◽  
pp. 229-244 ◽  
Author(s):  
R Batra ◽  
R B Barlow

The sensitivity of the Limulus lateral eye exhibits a pronounced circadian rhythm. At night a circadian oscillator in the brain activates efferent fibers in the optic nerve, inducing multiple changes in the physiological and anatomical characteristics of retinal cells. These changes increase the sensitivity of the retina by about five orders of magnitude. We investigated whether this increase in retinal sensitivity is accompanied by changes in the ability of the retina to process temporal information. We measured the frequency transfer characteristic (FTC) of single receptors (ommatidia) by recording the response of their optic nerve fibers to sinusoidally modulated light. We first measured the FTC in the less sensitive daytime state and then after converting the retina to the more sensitive nighttime state by electrical stimulation of the efferent fibers. The activation of these fibers shifted the peak of the FTC to lower frequencies and reduced the slope of the low-frequency limb. These changes reduce the eye's ability to detect rapid changes in light intensity but enhance its ability to detect dim flashes of light. Apparently Limulus sacrifices temporal resolution for increased visual sensitivity at night.


2015 ◽  
Vol 114 (6) ◽  
pp. 3234-3241
Author(s):  
Tchoudomira M. Valtcheva ◽  
Christopher L. Passaglia

Luminance and contrast adaptation are neuronal mechanisms employed by the visual system to adjust our sensitivity to light. They are mediated by an assortment of cellular and network processes distributed across the retina and visual cortex. Both have been demonstrated in the eyes of many vertebrates, but only luminance adaptation has been shown in invertebrate eyes to date. Since the computational benefits of contrast adaptation should apply to all visual systems, we investigated whether this mechanism operates in horseshoe crab eyes, one of the best-understood neural networks in the animal kingdom. The spike trains of optic nerve fibers were recorded in response to light stimuli modulated randomly in time and delivered to single ommatidia or the whole eye. We found that the retina adapts to both the mean luminance and contrast of a white-noise stimulus, that luminance- and contrast-adaptive processes are largely independent, and that they originate within an ommatidium. Network interactions are not involved. A published computer model that simulates existing knowledge of the horseshoe crab eye did not show contrast adaptation, suggesting that a heretofore unknown mechanism may underlie the phenomenon. This mechanism does not appear to reside in photoreceptors because white-noise analysis of electroretinogram recordings did not show contrast adaptation. The likely site of origin is therefore the spike discharge mechanism of optic nerve fibers. The finding of contrast adaption in a retinal network as simple as the horseshoe crab eye underscores the broader importance of this image processing strategy to vision.


1998 ◽  
Vol 80 (4) ◽  
pp. 1800-1815 ◽  
Author(s):  
Christopher L. Passaglia ◽  
Frederick A. Dodge ◽  
Robert B. Barlow

Passaglia, Christopher L., Frederick A. Dodge, and Robert B. Barlow. Cell-based model of the Limulus lateral eye. J. Neurophysiol. 80: 1800–1815, 1998. We present a cell-based model of the Limulus lateral eye that computes the eye's input to the brain in response to any specified scene. Based on the results of extensive physiological studies, the model simulates the optical sampling of visual space by the array of retinal receptors (ommatidia), the transduction of light into receptor potentials, the integration of excitatory and inhibitory signals into generator potentials, and the conversion of generator potentials into trains of optic nerve impulses. By simulating these processes at the cellular level, model ommatidia can reproduce response variability resulting from noise inherent in the stimulus and the eye itself, and they can adapt to changes in light intensity over a wide operating range. Programmed with these realistic properties, the model eye computes the simultaneous activity of its ensemble of optic nerve fibers, allowing us to explore the retinal code that mediates the visually guided behavior of the animal in its natural habitat. We assess the accuracy of model predictions by comparing the response recorded from a single optic nerve fiber to that computed by the model for the corresponding receptor. Correlation coefficients between recorded and computed responses were typically >95% under laboratory conditions. Parametric analyses of the model together with optic nerve recordings show that animal-to-animal variation in the optical and neural properties of the eye do not alter significantly its response to objects having the size and speed of horseshoe crabs. The eye appears robustly designed for encoding behaviorally important visual stimuli. Simulations with the cell-based model provide insights about the design of the Limulus eye and its encoding of the animal's visual world.


1974 ◽  
Vol 63 (5) ◽  
pp. 579-589 ◽  
Author(s):  
Robert B. Barlow ◽  
G. David Lange

Receptor units in the eye of the horseshoe crab are more sensitive to lateral inhibition at some levels of excitation than they are at others. As a result, the steady-state inhibition of the response of a given unit is not directly proportional to the response levels of neighboring units. This effect may be represented by the introduction of a nonlinearity in the Hartline-Ratliff system of equations. The nonlinear inhibitory effect appears to increase the operating range of the receptor units.


2005 ◽  
Vol 93 (3) ◽  
pp. 1611-1619 ◽  
Author(s):  
J. A. Borycz ◽  
J. Borycz ◽  
A. Kubów ◽  
R. Kostyleva ◽  
I. A. Meinertzhagen

Reliable estimates of the quantum size in histaminergic neurons are not available. We have exploited two unusual opportunities in the fly's ( Drosophila melanogaster) visual system to make such determinations for histaminergic photoreceptor synapses: 1) the possibility to microdissect successively from whole fly heads freeze-dried in acetone: the compound eyes; the first optic neuropils, or lamina; and the rest of the brain; and 2) the uniform sheaves of lamina synaptic terminals of photoreceptors R1–R6. We used this organization to count scrupulously the numbers of 30-nm synaptic vesicles from electron micrographs of R1–R6 profiles, and from microdissections we determined the regional contents of histamine in the compound eye, lamina, and central brain. Total head histamine averages 1.98 ng of which 9% was lost after freeze-drying in acetone and a further 28% after the brain was microdissected. Of the remainder, 71% was in the eye and lamina. Assuming that histamine loss from the tissue occurred mostly by diffusion evenly distributed among all regions, the overall lamina content of the head would be 0.1935 ng before dissection. From published values for the volumes of the brain's compartments, the computed regional concentrations of histamine are highest in the lamina (4.35 mM) because of the terminals of R1–R6. The concentration in the retina is ∼13% that in the lamina, suggesting that most histamine is vesicular. There are ∼43,500 ± 7,400 (SD) synaptic vesicles per terminal and, if all histamine is allocated equally and exclusively among these, the vesicle contents would be 858 ± 304 × 10−21 moles or ∼5,000 ± 1,800 (SD) molecules at an approximate concentration of 670 mM. These values are compared with the vesicle contents at synapses using acetylcholine and catecholamines.


1989 ◽  
Vol 71 (2) ◽  
pp. 244-253 ◽  
Author(s):  
T. A. Gennarelli ◽  
L. E. Thibault ◽  
R. Tipperman ◽  
G. Tomei ◽  
R. Sergot ◽  
...  

✓ A new model of traumatic axonal injury has been developed by causing a single, rapid, controlled elongation (tensile strain) in the optic nerve of the albino guinea pig. Electron microscopy demonstrates axonal swelling, axolemmal blebs, and accumulation of organelles identical to those seen in human and experimental brain injury. Quantitative morphometric studies confirm that 17% of the optic nerve axons are injured without vascular disruption, and horseradish peroxidase (HRP) studies confirm alterations in rapid axoplasmic transport at the sites of injury. Since 95% to 98% of the optic nerve fibers are crossed, studies of the cell bodies and terminal fields of injured axons can be performed in this model. Glucose utilization was increased in the retina following injury, confirming electron microscopic changes of central chromatolysis in the ganglion cells and increased metabolic activity in reaction to axonal injury. Decreased activity at the superior colliculus was demonstrated by delayed HRP arrival after injury. The model is unique because it produces axonal damage that is morphologically identical to that seen in human brain injury and does so by delivering tissue strains of the same type and magnitude that cause axonal damage in the human. The model offers the possibility of improving the understanding of traumatic damage of central nervous system (CNS) axons because it creates reproducible axonal injury in a well-defined anatomical system that obviates many of the difficulties associated with studying the complex morphology of the brain.


1982 ◽  
Vol 48 (2) ◽  
pp. 505-520 ◽  
Author(s):  
S. C. Chamberlain ◽  
R. B. Barlow

1. The retinotopic organization of retinal inputs from the lateral eye of Limulus to the optic ganglia of the brain was determined from microelectrode recordings of nerve impulses. 2. The central connections of the natural subunits of the lateral optic nerve were determined using cobalt impregnation of cut axons. 3. Complete retinal maps exist in both the lamina and medulla. The laminar map is a simple rotation and folding of the retinal array. The medullar map is more complex as a result of the combined effects of the chiasma and the basic subunit structure of the optic nerve, which is preserved in the lamina and medulla. 4. The chiasma between the lamina and medulla reverses the anterior-posterior axis of the retinal map. There is no corresponding reversal in the dorsal-ventral axis.


1978 ◽  
Vol 71 (6) ◽  
pp. 699-720 ◽  
Author(s):  
R B Barlow ◽  
A J Fraioli

Inhibition in the Limulus lateral eye in situ is qualitatively similar to that in the excised eye. In both preparations ommatidia mutually inhibit one another, and the magnitude of the inhibitory effects are linear functions of the response rate of individual ommatidia. The strength of inhibition exerted between single ommatidia is also about the same for both preparations; however, stronger effects can converge on a single ommatidium in situ. At high levels of illumination of the retina in situ the inhibitory effects are often strong enough to produce sustained oscillations in the discharge of optic nerve fibers. The weaker inhibitory influences at low levels of illumination do not produce oscillations but decrease the variance of the optic nerve discharge. Thresholds for the inhibitory effects appear to be determined by both presynaptic and postsynaptic cellular processes. Our results are consistent with the idea that a single ommatidium can be inhibited by more of its neighbors in an eye in situ than in an excised eye. Leaving intact the blood supply to the eye appears to preserve the functional integrity of the retinal pathways which mediate inhibition.


Sign in / Sign up

Export Citation Format

Share Document