Maintenance and repair of corneal stromal extracellular matrix (ECM) requires a tightly coordinated balance of ECM synthesis, degradation and remodeling in which proteolytic enzymes (proteinases) perform important functions. There are natural proteinase inhibitors present in preocular tear film (PTF) and cornea simultaneously with proteinases that prevent excessive degradation of normal healthy tissue. Disorders occur when there is an imbalance between proteinases and proteinase inhibitors in favor of the proteinases, causing pathologic degradation of stromal collagen and proteoglycans in the cornea. Two matrix metalloproteinases (MMPs), MMP-2 and MMP-9, are of major importance in terms of remodeling and degradation of the corneal stromal collagen. Immunohistochemical studies have shown different origins of MMP-2 and -9. MMP-2 is synthesized by corneal keratocytes and performs a surveillance function in the normal cornea, becoming locally activated to degrade collagen molecules that occasionally become damaged. Alternatively, MMP-9 may be produced by epithelial cells and polymorphonuclear neutrophils following corneal wounding. Because the cornea is in close contact with the preocular tear film (PTF), proteinases have been evaluated in the PTF. In damaged corneas, total proteolytic activity in the tear fluid was found to be significantly increased compared to normal eyes and contralateral eyes. Studies analyzing the proteolytic activity in serial PTF samples during corneal healing led to the following conclusions: ulcerative keratitis in animals is associated with initially high levels of tear film proteolytic activity, which decrease as ulcers heal; proteinase levels in melting ulcers remain elevated leading to rapid progression of the ulcers. The success of medical and surgical treatment of the corneal ulcers is reflected by the proteolytic activity in tears. In animals, successful treatment leads to a rapid reduction in tear film proteolytic activity that corresponds with the improvement in the clinical signs of corneal ulceration. The in vitro effects of various compounds on proteolytic activity in the tear fluid of animals with ulcerative keratitis have been evaluated and their important inhibitory effects have been confirmed. Because these various compounds utilize different mechanisms to inhibit various families of proteinases, a combination of these proteinase inhibitors may be beneficial.

Proteinases of the cornea and preocular tear film

It has recently been shown that some non-human animals can cross-modally recognize members of their own taxon. What is unclear is just how plastic this recognition system can be. In this study, we investigate whether an animal, the domestic horse, is capable of spontaneous cross-modal recognition of individuals from a morphologically very different species. We also provide the first insights into how cross-modal identity information is processed by examining whether there are hemispheric biases in this important social skill. In our preferential looking paradigm, subjects were presented with two people and playbacks of their voices to determine whether they were able to match the voice with the person. When presented with familiar handlers subjects could match the specific familiar person with the correct familiar voice. Horses were significantly better at performing the matching task when the congruent person was standing on their right, indicating marked hemispheric specialization (left hemisphere bias) in this ability. These results are the first to demonstrate that cross-modal recognition in animals can extend to individuals from phylogenetically very distant species. They also indicate that processes governed by the left hemisphere are central to the cross-modal matching of visual and auditory information from familiar individuals in a naturalistic setting.

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2012.0626

Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans.

Laterality and emotions: Visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value

We have established that lateral biases are characteristic of visual behaviour in 65 horses. Two breeds, Trotters and French Saddlebreds aged 2 to 3, were tested on a novel object test. The main finding was a significant correlation between emotionality index and the eye preferred to view the novel stimulus: the higher the emotionality, the more likely that the horse looked with its left eye. The less emotive French Saddlebreds, however, tended to glance at the object using the right eye, a tendency that was not found in the Trotters, although the emotive index was the same for both breeds. The youngest French Saddlebreds did not show this trend. These results are discussed in relation to the different training practices for the breeds and broader findings on lateralisation in different species.

Laterality of horses associated with emotionality in novel situations

We investigated whether horses display greater reactivity to a novel stimulus presented in the left compared to the right monocular visual field, and whether a population bias exists for escape turning when the same stimulus was presented binocularly. Domestic horses (N=30) were tested on three occasions by a person opening an umbrella five metres away and then approaching. The distance each horse moved away before stopping was measured. Distance was greatest for approach on the left side, indicating right hemisphere control of flight behaviour, and thus followed the same pattern found previously in other species. When order of monocular presentation was considered, an asymmetry was detected. Horses tested initially on the left side exhibited greater reactivity for left approach, whereas horses tested on the right side first displayed no side difference in reactivity. Perhaps left hemisphere inhibition of flight response allowed horses to learn that the stimulus posed no threat and this information was transferred to the right hemisphere. No population bias existed for the direction of escape turning, but horses that turned to the right when approached from the front were found to exhibit longer flight distances than those that turned to the left.

Asymmetry of flight and escape turning responses in horses

The optic nerve is divided in four regions: intraocular, intraorbital, intracanalicular, and intracranial. The vertebrate retinal ganglion cells are classified by morphology, physiology and soma size. Species differences and similarities occur with retinal ganglion cells. Alpha retinal ganglion cells have large somata, large dendritic fields, large-diameter axons, and are most dense in the peripheral retina. Beta retinal ganglion cells have smaller diameter somata, smaller dendritic fields, small diameter axons, and predominate in the central retina. Gamma retinal ganglion cells are a heterogenous class of cells and have small diameter axons, and slow axon conduction velocities. The spatial distribution and organization of the retinal ganglion cells extends retinotopically through the nerve fiber layer, optic nerve, optic chiasm, optic tract, lateral geniculate nucleus, and visual cortex. The retinal nerve fiber layer thickness decreases from the optic disk toward the periphery of the retina. The retrobulbar optic nerve axon counts and axon density vary by species, with larger nerves having higher axon counts. Decussation of the optic nerve axons at the optic chiasm varies with 100% decussation in most birds and fish, 65% in cats, 75% in dogs, 80–90% in large animals, and 50% in primates. Centrifugal axons also occur in the optic nerve and may represent a method by which the brain can influence retinal activity.

Comparative retinal ganglion cell and optic nerve morphology

The axoplasm of optic nerve axons moves bidirectionally at various speeds along an intra-axonal pressure gradient from the retinal ganglion cell (RGC) somata toward its synapse, and from the synapse towards the RGC somata. The axoplasmic flow of optic nerve axons is precarious even at normal intraocular pressures (IOP) as it moves from the intraocular optic nerve through the scleral lamina cribrosa to the intraorbital optic nerve. The scleral lamina cribrosa is not simply a porous region of the sclera but a specialized extracellular matrix of the central nervous system whose movement during fluctuations in IOP can affect optic nerve axoplasmic flow. The abundant optic nerve blood supply maintains adequate optic nerve head perfusion through a process of vascular autoregulation. Glaucoma is associated with reduced optic nerve axoplasmic flow and compromised optic nerve circulation such that RGC death due to glutamate excitotoxicity and neurotrophin deprivation result.

Comparative optic nerve physiology: implications for glaucoma, neuroprotection, and neuroregeneration.

Ulcerative keratitis is a common and potentially blinding ocular disease of horses, capable of progressing to corneal perforation in as little as 24 h. This rapid stromal degeneration is mediated in part by exogenous and endogenous proteinases. We measured and compared the concentrations of two matrix metalloproteinases (MMP-2 and MMP-9) and a serine proteinase (neutrophil elastase) present in the precorneal tear film of normal horses and horses with rapidly progressing ulcerative keratitis. Precorneal tear film samples were collected from 23 ulcerated and 21 unaffected eyes of 23 horses with unilateral ulcerative keratitis, and from 33 normal eyes of 17 control horses. MMP-2, MMP-9, and neutrophil elastase were identified by casein and gelatin zymography and quantified by computerized image analysis. Median MMP-9 levels were significantly higher in the precorneal tear film of young control horses vs. older control horses (P= 0.005). Median MMP-2, MMP-9, and neutrophil elastase levels were significantly higher in the precorneal tear film of ulcerated eyes when compared to age-matched normal controls (P= 0.004, P= 0.001, and P= 0.012, respectively). Median MMP-2 levels were also significantly higher in the precorneal tear film of contralateral eyes of affected horses when compared to age-matched normal controls (P= 0.004). No significant differences in median proteinase levels were detected between ‘sterile’ ulcers and those from which bacteria or mixed infections (bacteria and fungi) were isolated. However, median MMP-2 and neutrophil elastase levels were significantly higher in the precorneal tear film of eyes with ‘sterile’ ulcers when compared with ulcerated eyes from which fungi were isolated (P < 0.05). The results of this study support the use of topical antiproteinase therapy which targets both MMPs and serine proteinases in progressive equine ulcerative keratitis.

Evaluation of tear film proteinases in horses with ulcerative keratitis.

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Comparative retinal ganglion cell and optic nerve morphology

Comparative optic nerve physiology: implications for glaucoma, neuroprotection, and neuroregeneration.

Evaluation of tear film proteinases in horses with ulcerative keratitis.