Anatomical and functional evidence for progressive age-related decline in parasympathetic control of choroidal blood flow in pigeons.

The choroid receives extensive parasympathetic innervation, which in birds arises largely from the ciliary ganglion (CG). Since age-related changes in parasympathetic regulation of choroidal blood flow (ChBF) could contribute to age-related retinal decline, we used anatomical and functional methods to determine if ChBF control by the CG shows age-related decline in pigeons. The efficacy of the choroidal vasodilatory response to activation of the CG preganglionic input from the medial subdivision of the nucleus of Edinger-Westphal (EWM) was assessed using laser Doppler flowmetry (LDF). The EWM receives bisynaptic retinal input, and electrical stimulation of EWM or light stimulation of the retina in young animals produces dramatic choroidal vasodilation. Transcleral LDF was therefore used to measure both basal ChBF and the increases in ChBF elicited by electrical stimulation of EWM or by retinal illumination in 0.5-18 year old pigeons. Fixed cryostat sections of the eye from 0.5 to 22 year old pigeons were immunolabeled for the 3A10 neurofilament-associated antigen to determine if intrachoroidal nerve fibers arising from CG exhibited age-related loss. We focused on superior choroid, since it is the primary target for CG nerve fibers. There was a marked age-related loss in the ChBF vasodilatory response elicited by either EWM stimulation or retinal illumination, as was also true for basal ChBF. A progressive decrease in choroidal nerve fibers of CG origin, to 17% of youthful abundance by 22 years of age, was also observed. The evoked ChBF increase, and basal ChBF, achieved 50% of their age-related decline between the ages of 3 and 4 years, while half the loss in CG innervation of choroid was later, occurring by 10 years. Age-related loss of choroidal nerve fibers occurs in parallel with but more slowly than the reduction in basal ChBF and the choroidal vasodilation that can be elicited via natural (light) or electrical activation of the central neural input to CG choroidal neurons. The prominent age-related decline in parasympathetic control of ChBF early in the pigeon life span could contribute to the age-related retinal decline observed in pigeons.

Functional and morphological assessment of age-related changes in the choroid and outer retina in pigeons.

We sought to determine if choroidal and outer retinal deterioration occur with age in pigeons, as they do in other species, and investigated the relationship between age-related retinal and choroidal changes. In 64 pigeons ranging in age over the pigeon lifespan (0.5-20 years), we measured some or all among the following parameters: choroidal blood flow (ChBF) by laser Doppler flowmetry, choroidal thickness and choriocapillary vessel abundance by LM histology, choriocapillary endothelial cell transport specializations by EM histology, acuity by behavioral methods, and degenerating photoreceptor abundance and total photoreceptor abundance by LM histology. Regression and Receiver Operator Curve (ROC) analyses were used to characterize the pattern of age-related changes and determine the ages at or by which significant changes occurred. For the 45 birds for which we measured choroidal parameters, choriocapillary vessel abundance showed a curvilinear decline with age and half of this decline occurred by 3.5-4.6 years. The endothelial cell transport specializations called channels also declined curvilinearly with age. Choroidal thickness was slightly increased between the ages of 3-6 years, and thereafter declined steadily so that choroidal thickness in the oldest birds was half that in the youngest. ChBF showed an abrupt decline of about 20% at 4 years and a further 20% decline thereafter. In the 53 birds for which we obtained visual acuity and/or photoreceptor data, we observed a curvilinear decline in acuity (with half the decline having occurred by 8 years) and a prominent stepwise decline of about 20% in photoreceptor abundance at 4.7 years, followed by further decline thereafter. The period of major photoreceptor loss coincided with ages during which about 10% of photoreceptors appeared to show degenerative changes (4-8 years of age). Using partial correlation analysis with the common effect of age held constant, ChBF was found to have a positive correlation with acuity. Our results show that ChBF and choroidal vascularity decline significantly with age in pigeons, as do acuity and photoreceptor abundance. Our statistical analyses suggest that prominent choroidal vascular decline preceded the visual decline, and that there is a positive relationship between choroidal and visual functions. Thus, our findings are consistent with the view that age-related decline in choroidal function might contribute to age-related vision loss in pigeons.

Can rats acquire an olfactory learning set?

Experimental rats were trained on multiple 2-odor discrimination tasks, whereas controls were given repeated sessions on Task 1 and then were tested on a novel 2-odor task. Experimental rats showed strong positive transfer across problems and approached errorless or near-errorless learning. Control rats maintained near-perfect performance on Task 1 but performed at chance on initial trials when tested with novel odors. Thus, the near-errorless terminal performance of experimental rats was a function their having been trained on multiple problems and was not simply the result of eliminating "disruptive response tendencies" (I. C. Reid & R. G. M. Morris, 1992). Results support the view that when rats are trained on a series of 2-odor discrimination tasks, they acquire a strategy or rule that allows them to solve new problems with few or no errors.

Avian behavioural neuroscience: past, present and future perspectives.

A survey of avian brain-behavior conference reports of the last 25 years reveals that neither the avian species studied nor the types of scientific questions asked have changed very much since the first such conference report in 1974. The birds studied tend, for the most part, to be pigeons, chickens, quail, and canaries. Because of the growing interest in avian vocalization and its neural control, one recent conference featured studies of canaries, zebra finches, and budgerigars. The topics of investigation at these conferences largely have involved sensory systems, mostly sensory and sensorimotor mechanisms with a heavy emphasis on vision and audition, as well as studies of learning and memory. Future research should expand the range of orders and species of birds studied so as to shed light on evolutionary trends within Aves as a whole. The scope of behavioral questions asked also should be broadened to include topics of neuroethological interest.

Visual acuity losses in pigeons with lesions of the nucleus of Edinger-Westphal that disrupt the adaptive regulation of choroidal blood flow.

Choroidal blood flow (ChBF) in birds is regulated by a neural circuit whose components are the retina, the suprachiasmatic nucleus, the medial division of the Edinger-Westphal nucleus (EWM), the ciliary ganglion, and the choriod. We have previously shown that lesions of EWM appear to result in pathological alterations in the retina. To determine whether EWM lesions also lead to altered visual functions, we have examined the effects of EWM lesions on visual acuity in pigeons. Bilateral lesions of EWM were made electrolytically, and visual acuity for high-contrast, square-wave gratings was determined behaviorally about 1 year later and compared to that of a group of pigeons that had received sham lesions of EW about 1 year prior to acuity testing. Because lesions targeting EWM invariably resulted in damage to the adjoining lateral part of the Edinger-Westphal nucleus (EWL), which controls pupillary constriction and accommodation, two additional control groups were studied. In one such control group, bilateral lesions in the area pretectalis (AP), which innervates the pupillary control part of EWL and thereby controls pupillary constriction, were made and the effects on visual acuity determined about 1 year later. In the second such control group, the effects of acute accommodative and pupillary dysfunction on acuity were studied in pigeons made cycloplegic. The accuracy of all lesions was later confirmed histologically. The mean acuities of birds with AP lesions (9.1+/-1.4 cycles/deg) and sham lesions (7.1+/-1.5 cycles/deg) were not significantly different from normal, based on published normative data on pigeons. In contrast, pigeons with lesions that completely destroyed EW bilaterally showed visual acuity (2.7+/-0.1 cycles/deg) that was well below the acuity of the sham and AP-lesion control groups. The acuity of the cycloplegic pigeons (4.8+/-0.3 cycles/deg) and one pigeon with a nearly complete bilateral EWL but a unilateral EWM lesion (6.4 cycles/deg) indicated that only about half of the loss with a bilateral EW lesion could be attributed to accommodative dysfunction. Thus, bilateral destruction of EWM appears to have led to a loss in visual acuity. This conclusion suggests that disruption of adaptive neural regulation of ChBF may impair visual function. Destruction of EWM was, however, associated with damage to the somatic components of the oculomotor and trochlear nuclei. The possibility cannot be excluded that such damage also contributed to the acuity loss.

Color reversal-learning deficits after tectofugal pathway lesions in the pigeon telencephalon.

Pigeons were post-operatively trained to discriminate two colors presented simultaneously. After reaching criterion on this task, they were required to perform a series of reversals of the color discrimination in which the positive and negative consequences of the stimuli were interchanged. Lesions of ectostriatum (the telencephalic target of the avian tectofugal visual pathway) impaired the ability of pigeons to learn a color-reversal task. An examination of the pattern of sparing and loss of performance on this task after lesions of various components of the ascending visual pathways suggests that deficits in color-reversal learning observed after lesions of the visual Wulst are not due to the Wulst's connections with the thalamofugal pathway. Instead, the data suggest that the visual Wulst maintains a role in color-reversal learning through its connections with the tectofugal pathway.

Evolution of sensory pathways in vertebrates.

Sensory receptor evolution is a function of the array of events in the physical world that are detectable by biological systems. Examples of both conservation and innovation occur across vertebrates in the organization of sensory systems for the reception of photic, positional, chemical, tactile, mechanosensory and electrosensory lateral line, acoustic, and magnetic stimuli. Recent findings in genetics and ontogeny allow new approaches to questions of how new sensory receptors and their corresponding central nervous system pathways evolve, how sensory specialization arises and its effects on other sensory systems, the role of cell-adhesion molecules in the ontogeny of sensory pathways and their topological organization, and the occurrence of reorganization and co-option of developmental modules over sensory system evolution. Relatively simple alterations at the genetic and ontogenetic levels often can result in alterations in the phenotype of far greater complexity.

Hyperstriatum ventrale in pigeons: effects of lesions on color-discrimination and color-reversal learning.

Previous lesion studies of color-reversal learning in pigeons show that an impairment results when (1) the tectofugal visual pathway is damaged at either the thalamic level (nucleus rotundus) or the telencephalic level (ectostriatum), or (2) the thalamofugal visual pathway is damaged at the telencephalic level (the visual Wulst). An impairment does not result, however, when the thalamic source of thalamofugal input (n. opticus principalis thalami or OPT) to the visual Wulst is damaged. These results suggest that the visual Wulst plays a role in color-reversal learning as a consequence of visual information routed from the tectofugal pathway via other visual areas in the telencephalon. One such area is the hyperstriatum ventrale (HV). In the present study, after ablation of the medial and lateral regions of HV, pigeons were trained postoperatively to discriminate between two colors presented simultaneously. After reaching criterion, the pigeons were required to perform a series of discrimination reversals in which the positive and negative stimuli were interchanged. Lesions of medial HV resulted in impaired performance of a color-discrimination task (i.e. original learning), but did not affect discrimination reversal. An impairment in color-reversal learning resulted from combined damage to lateral HV and the fronto-thalamic tract (FT), which carries ascending visual input from OPT to the visual Wulst. No deficits were observed when either lateral HV or FT were damaged alone. These findings suggest that both the thalamofugal and tectofugal pathways provide the visual Wulst with visual input relevant to color-reversal learning.

Scleral matrix metalloproteinases, serine proteinase activity and hydrational capacity are increased in myopia induced by retinal image degradation.

In the avian model of myopia, retinal image degradation quickly leads to ocular enlargement. We now give evidence that regionally specific changes in ocular size are correlated with both biomechanical indices of scleral remodeling, e.g. hydration capacity and with biochemical changes in proteinase activities. The latter include a 72 kDa matrix metalloproteinase (putatively MMP-2), other gelatin-binding MMPs, an acid pH MMP and a serine protease. Specifically, we have found that increases in scleral hydrational capacity parallel increases in collagen degrading activities. Gelatin zymography reveals that eyes with 7 days of retinal image degradation have elevated levels (1.4-fold) of gelatinolytic activities at 72 and 67 kDa M(r) in equatorial and posterior pole regions of the sclera while, after 14 days of treatment, increases are no longer apparent. Lower M(r) zymographic activities at 50, 46 and 37 kDa M(r) are collectively increased in eyes treated for both 7 and 14 days (1.4- and 2.4-fold respectively) in the equator and posterior pole areas of enlarging eyes. Western blot analyses of scleral extracts with an antibody to human MMP-2 reveals immunoreactive bands at 65, 30 and 25 kDa. Zymograms incubated under slightly acidic conditions reveal that, in enlarging eyes, MMP activities at 25 and 28 kDa M(r) are increased in scleral equator and posterior pole (1.6- and 4.5-fold respectively). A TIMP-like protein is also identified in sclera and cornea by Western blot analysis. Finally, retinal-image degradation also increases (approximately 2.6-fold) the activity of a 23.5 kDa serine proteinase in limbus, equator and posterior pole-sclera that is inhibited by aprotinin and soybean trypsin inhibitor. Taken together, these results indicate that eye growth induced by retinal-image degradation involves increases in the activities of multiple scleral proteinases that could modify the biomechanical properties of scleral structural components and contribute to tissue remodeling and growth.

Color-reversal learning: effects after lesions of thalamic visual structures in pigeons.

The performance of pigeons on a color-reversal learning task was assessed after thalamic lesions disrupting the thalamofugal and tectofugal visual pathways. Successful performance of a simultaneous color discrimination was accomplished after surgery, and a series of reversals of the original discrimination followed during which the positive and negative consequences associated with the stimuli were interchanged. Shimizu and Hodos (1989) had reported that lesions of two laminae in the visual wulst (IHA and HD), both targets of the avian thalamofugal pathway, resulted in increased errors in a color-reversal learning task in pigeons. This finding suggested that the thalamofugal pathway might play a role in visual discrimination involving stimulus context changes. In the present study, lesions of the OPT complex (the thalamic source of afferents to IHA and HD) were found to have no effect on color-reversal learning performance. Instead, we found that damage to nucleus rotundus (the thalamic component of the tectofugal pathway) resulted in deficits that were far in excess of those that had been obtained after IHA and HD lesions. We suggest that the color-reversal learning deficits after Wulst lesions are not due to the Wulst's connections with the thalamofugal pathway, but rather to its connections with the tectofugal pathway.

Thermal gradients in the eyes of lid-sutured chicks.

Thermal gradients were measured from the cornea to the posterior pole in the eyes of 11 chicks, six of which had the lids of one eye sutured three weeks previously. A comparison was made between eyes that were chronically closed by lid-suture (while still sutured shut) and two types of control eyes: (a) treated controls, which were the non-sutured, contralateral eyes of the lid-sutured chicks and (b) untreated controls, which were the eyes of a different group of chicks in which neither eye had been sutured. The results indicated that transient closing of the eyes of normal, untreated chicks (untreated controls) elevated the ocular temperature by about 1.5 degrees C at the cornea; the extent of thermal elevation diminished as the thermoprobe was advanced towards the posterior pole. In contrast, when the transiently closed eyes in untreated control chicks were compared with the chronically closed eyes of the lid-sutured chicks, the lid-sutured eyes were cooler by 2 degrees - 2.5 degrees. When the sutured lids were opened, however, the eyes were isothermal with the untreated control eyes. Moreover, the eyes of lid-sutured chicks were isothermal with their contralateral, non-sutured, control eyes (treated control), whether in the opened or closed state. A comparison of the untreated control eyes and the treated control eyes revealed no differences (except at the cornea) when the eyes were opened; but when the eyes were closed, the treated control eyes were 2 degrees - 3 degrees cooler than the untreated control eyes.(ABSTRACT TRUNCATED AT 250 WORDS)

Reduction in choroidal blood flow occurs in chicks wearing goggles that induce eye growth toward myopia.

Goggles that degrade the retinal image produce axial enlargement of the ocular globe and large myopic refractive errors. Many authors have assumed that visual image degradation itself leads to myopia. Hodos and co-authors have shown, however, that goggled eyes in chicks are considerably warmer than normal. Such temperature changes may either underlie or be a consequence of alterations in choroidal blood flow (CBF). Since alterations in CBF could affect eye growth, we explored the effect of monocular goggling on CBF in chicks. Plastic goggles were glued over one eye in four-day old chicks and the goggles were left in place for 12 or 14 days. Fourteen days after the goggling, CBF was measured using laser Doppler velocimetry. Three groups of chicks were studied: 1) chicks with goggles for 14 days; 2) chicks with goggles for 12 days followed by no goggles for the two days; 3) age matched non-goggled chicks. A -scan ultrasonography confirmed that the visual deprivation produced vitreous chamber elongation in the goggled eye and that the degree of elongation for the goggled eye was the same for the two goggled groups. The results were: 1) blood flow in non-goggled chicks was similar in both eyes; 2) blood flow was significantly reduced in the goggled eye in chicks wearing goggles for 14 days- 37% of control; and 3) blood flow was still significantly reduced in the goggled eye in chicks whose goggles were removed two days before measurement- 51% of control. These results show that CBF is reduced by goggles that result in myopic eye growth.(ABSTRACT TRUNCATED AT 250 WORDS)

Visual performance of pigeons following hippocampal lesions.

The effect of hippocampal lesions on performance in two psychophysical measures of spatial vision (acuity and size-difference threshold) was examined in 7 pigeons. No difference between the preoperative and postoperative thresholds of the experimental birds was found. The visual performance of pigeons in the psychophysical tasks failed to reveal a role of the hippocampal formation in vision. The results argue strongly that the behavioral deficits found in pigeons with hippocampal lesions when tested in a variety of memory-related spatial tasks is not based on a defect in spatial vision but impaired spatial cognition.

Age-dependent intensity-difference thresholds in pigeons.

Recent studies have reported age-related deficits in visual acuity and changes in retinal morphology in pigeons. The experiment reported here was designed to determine the effects of age on intensity difference thresholds in pigeons. Six subjects, age 2-17 yr, were trained to discriminate between two stimuli that differed in luminance. When this training was complete, the subjects were presented with a series of stimulus comparisons ranging from 0.08 to 0.43 log unit. Threshold was calculated by determining the luminance difference that corresponded to 75% correct. These data were pooled with 56 intensity-difference thresholds that had been collected from pigeons of various ages over a 20 yr period using the same procedure. A regression analysis that was performed on the pooled data set gave the result b = 0.0038, d.f. = 61 P < 0.05, r2 = 0.066 which indicates that age accounted for approx. 7% of the variance in intensity-difference threshold. This finding, although statistically significant, indicates that as pigeons age their ability to perform this type of non-spatial discrimination task is not greatly impaired. This finding suggests that deficits associated with a spatial visual task in pigeons, such as visual acuity, are task specific and are not due to a global performance deficit.

The Scala naturae revisited: evolutionary scales and anagenesis in comparative psychology.

Recent suggestions that evolutionary scales have a place in theorization about the evolution of behavior have been based on the concept of anagenesis, formerly associated with notions of biological progress. An associated concept is that of grades, often used as units of anagenetic advance. Advocates of anagenetic analysis in comparative psychology cite the writings of biologists Bernard Rensch, Julian Huxley, George Gaylord Simpson, and Stephen Jay Gould to support the usefulness of anagenesis but treat the positions of each of these theorists as if they were the same. In fact, they differ considerably in their definition of anagenesis and in its application to specific issues in evolution. The anagenetic approach is criticized as axiological and frequently anthropocentric. Although the formation of grades can be useful, a sequence of grades must not be assumed to represent historical stages in the evolution of specific structures or behaviors.

Intraocular pressure and eye enlargement in chicks.

In chicks, the application of optical devices that blur vision results in eye enlargement and ametropia. The research presented here investigated changes in intraocular pressure (IOP), specifically intravitreal pressure, that occur with eye enlargement induced by this means. Plastic goggles (domes) were glued over one eye in 25 domestic chicks. Plastic rings were glued around one eye in 25 control chicks to control for the mechanical effects of the treatment but which left their vision undisturbed. Following two weeks of treatment, domes and rings were removed and IOP was measured. Mean IOP of the domed eyes was 1.14 mm Hg lower than that of control eyes, a difference that was not statistically significant. The eyes of an additional group of 20 chicks that experienced similar treatments were refracted; these refractions revealed that the dome-treated eyes had a mean refractive state that was 7.98 D myopic relative to the ring controls, which was statistically significant. The results indicate that IOP does not change significantly in chicks with experimental eye enlargement induced by retinal-image degradation.

Electroretinographic changes in aged pigeons.

Photopic electroretinograms, either to full-field light flashes (FERGs) or to contrast-reversal of square-wave gratings (PERGs) have been recorded in pigeons aged 2 years old (n = 5) and 10 years old (n = 5). Mydriatic pupil diameter, ophthalmoscopic appearance of the retinal fundus and optic media, and refractive state were comparable in the two groups. V/log I functions of individual FERG components (a-wave, b-wave and oscillatory potentials) displayed significantly lower slopes in the old birds than in the young, which suggests a reduction in retinal gain. PERG amplitude also was significantly lower in the older birds over a wide range of spatial frequencies (0.2-8.8 c/deg). Estimated visual acuity based on the extrapolated high-frequency cut off was 18 c/deg in the younger birds and 7.8 c/deg in the older birds. These results are in agreement with psychophysical data and retinal age-related losses in visual acuity, photoreceptors and retinal ganglion cells. Since these findings are comparable to those reported for humans, the results suggest that pigeons may serve as a useful model for human visual aging.

Age-dependent changes in visual acuity and retinal morphology in pigeons.

The visual acuities of 17 pigeons that ranged in age from 2 to 17 years were tested with high-contrast, square-wave gratings. A systematic decline in visual acuity was observed that was well described by a logarithmic function. Pupillary diameter also declined with age, which decreased retinal illumination, but increased depth of focus. A small amount of presbyopia also was observed. Both the decrease in retinal illumination and the presbyopia accounted for only a trivial proportion of the acuity loss. No relationship between corneal or lenticular density and age was observed. Ophthalmoscopic examination of the optic media revealed no abnormalities associated with age. Microscopic examination of the area dorsalis of the retina (the high-density region specialized for frontal vision) revealed age-related losses of up to 33% of photoreceptors and 23% of cells in the ganglion-cell layer. A study of the photoreceptor layer within area dorsalis indicated that single-cone densities were unaffected by aging whereas the double-cone densities, which are the predominant photoreceptor type in the area dorsalis, were reduced in number by about one third. Calculation of the Nyquist limit both for photoreceptors and ganglion cells suggested that the decreased retinal density together with the decreased retinal illumination and presbyopia could not account for all of the observed acuity loss.

Lower-field myopia in birds: an adaptation that keeps the ground in focus.

In the lower visual field of pigeons, a myopia (near-sightedness) has been reported that progressively increases with the angle below the horizon. Previous data suggested that this lower-field myopia may be an adaptation that permits pigeons to keep the ground in focus while they forage, and simultaneously, to monitor the horizon and sky for predators. We report here a lower-field myopia in other species of birds that have a wide range of heights. A geometric model of this adaptation predicts that the amount of myopia should be systematically related to the distance from the pupil to the ground. The eyes of quail, chickens and cranes of various heights (7.0-104.1 cm) were refracted at 60 deg below the horizon. Their myopia was close to the predicted value at each height.