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The Vertebrate Eye and Its Adaptive Radiation.

How are the functions performed by one part of the nervous system integrated with those of another? This fundamental issue pervades virtually every aspect of brain function from sensory and cognitive processing to motor control. Yet from a physiological perspective we know very little about the neural mechanisms underlying the integration of distributed processes in the nervous system. Even the simplest of sensori-motor acts engages vast numbers of cells in many different parts of the brain. Such actions require coordination between a host of neural systems, each of which must carry out parallel computations involving large populations of interconnected neurons. It seems reasonable to assume that a mechanism or class of mechanisms has evolved to temporally coordinate the activity within and between subsystems of the central nervous system. For several reasons, neuronal rhythms have long been thought to play an important role in such coordination. Since the discovery of the Electroencephalogram (EEG) over 60 years ago it has been known that a number of structures in the mammalian brain engage in rhythmic activities. These patterned neuronal oscillations take many forms. They occur over a broad range of frequencies, and are present in a multitude of different systems in the b~ain, during a variety of different behavioral states. They are often the most salient aspect of observable electrical activity in the brain and typically encompass widespread regions of cerebral tissue. With the advent of new techniques of multielectrode recording and neural imaging, it is now within the realm of possibility 'to record from 100 single neurons simultaneously (Wilson and McNaughton, 1993), to optically measure the activity in a cortical area (Blasdel and Salama, 1986; T'so et al., 1990), or to noninvasively image the pattern of electric current flow in an alert human being performing a task (Pantev et al., 1991). These new techniques have revealed that spatially and temporally organized activity among distributed populations of cells often takes the form of synchronous rhythms. When combined with cellular neurophysiological and anatomical studies these findings provide new insights into the behavior and mechanisms controUing the coordination of activity in neuronal populations.

Synchronous oscillations in neuronal systems: mechanisms and functions.

Using high-resolution adaptive-optics imaging combined with retinal densitometry, we characterized the arrangement of short- (S), middle- (M), and long- (L) wavelength-sensitive cones in eight human foveal mosaics. As suggested by previous studies, we found males with normal color vision that varied in the ratio of L to M cones (from 1.1:1 to 16.5:1). We also found a protan carrier with an even more extreme L:M ratio (0.37:1). All subjects had nearly identical S-cone densities, indicating independence of the developmental mechanism that governs the relative numerosity of L/M and S cones. L:M cone ratio estimates were correlated highly with those obtained in the same eyes using the flicker photometric electroretinogram (ERG), although the comparison indicates that the signal from each M cone makes a larger contribution to the ERG than each L cone. Although all subjects had highly disordered arrangements of L and M cones, three subjects showed evidence for departures from a strictly random rule for assigning the L and M cone photopigments. In two retinas, these departures corresponded to local clumping of cones of like type. In a third retina, the L:M cone ratio differed significantly at two retinal locations on opposite sides of the fovea. These results suggest that the assignment of L and M pigment, although highly irregular, is not a completely random process. Surprisingly, in the protan carrier, in which X-chromosome inactivation would favor L- or M-cone clumping, there was no evidence of clumping, perhaps as a result of cone migration during foveal development.

https://www.jneurosci.org/content/jneuro/25/42/9669.full.pdf

Organization of the Human Trichromatic Cone Mosaic

Functional architecture of the retina: Development and disease

Cobaltous-lysine was applied to one optic nerve of normal goldfish in order to determine the source of the centrifugal innervation of the retina. Cobalt-filled cells were not observed in the optic tectum, pretectum, thal-amus, or hypothalamus. However, filled cells were observed outside the central nervous system either interspersed between the olfactory nerve fibers orrostrally along the ventromedial aspect of the olfactory bulbs. These cells appear to correspond to the ganglion cells of the nervus terminalis. The cells were located bilaterally and had dendrites that branched in close proximity to the cell body and axons that coursed caudally through the medial olfactory tract. The axons traveled in the ventral forebrain and entered the optic tracts. The axons also gave off fine branches that appeared to terminate in the vicinity of the anterior commissure and in the preoptic region. Application of cobaltous-lysine to a cut olfactory tract resulted in cobalt-filled fibers in the optic tracts, retinal optic fiber layer, and retinal ganglion cell layer. However, the precise terminations of these fibers within the retina could not be readily established. The results are discussed with respect to the plethora of sources of retinopetal cells observed by others in fish and with respect to the innervation of the retina by luteinizing hormone-releasing hormone axons.

Centrifugal innervation of goldfish retina from ganglion cells of the nervus terminalis

Cobaltous lysine applied to the distal stump of a severed opticnerve was used to study the retinal projections of normal adult goldfish. Both the termination areas of optic axons and the pathways they traveled were established. Contrary to previous descriptions of the goldfish visual system, the optic nerves do not decussate completely at the optic chiasm. Fascicles that entered the ipsilateral optic tract innervated targets in the ipsilateral thalamus and optic tectum. Other optic fibers crossed the posterior commissure from the contralateral side of the brain and also innervated the ipsilateral tectum and thalamus. In addition, optic fibers bilaterally innervated a hypothalamic target in close proximity to the infundibulum that may correspond to the nucleus tuberis lateralis. The contralateral preoptic region contained two discrete areas of innervation, each served by separate fascicles. The ipsilateral preoptic region was similarly innervated, but more sparsely. Fibers that entered the contralateral ventral thalamus originated from three fascicles and terminated in three distinct targets. In contrast, three targets in the contralateral dorsal thalamus were served by one fascicle, and fibers passed from one nucleus to the other two. Innervation of the ipsilateral thalamus was similar to that seen contralaterally. Each main optic tract divided into three tracts, two of which entered the optic tectum, while the other innervated several pretectal areas. Other fibers innervated an accessory optic nucleus located near nucleus glomerulosus. The contralateral tectum contained numerous radially oriented optic fascicles. These fascicles represented optic fibers that left thalamic and pretectal targets to enter the optic tectum from beneath the stratum periventriculare. Optic fibers were also observed in the transverse commissure, tractus rotundus, horizontal commissure, tractus rotundus, horizontal commissure, tectobulbar tract, and fasciculus retroflexus. Therefore, it appears that many of the anomalous projections seen after tectal ablation or after optic nerve crush are not in fact aberrant. Such projections probably reflect the presence of unusually large numbers of optic fibers in tracts that normally contain optic axons, as well as increased innervation of areas that normally receive sparse retinal projections. Filled tectal cells that could represent cells projecting to the retina were not observed in either tectal lobe. The ipsilateral retinal projections could not be attributed to cobaltouslysine being transneuronally transported in readily detectable amounts.

Retinal projections in the goldfish: A study using cobaltous‐lysine

Most primate retinas have an area dedicated for high visual acuity called the fovea centralis. Little is known about specific mechanisms that drive development of this complex central retinal specialization. The primate area of high acuity (AHA) is characterized by the presence of a pit that displaces the inner retinal layers. Virtual engineering models were analyzed with finite element analysis (FEA) to identify mechanical mechanisms potentially critical for pit formation. Our hypothesis is that the pit emerges within the AHA because it contains an avascular zone (AZ). The absence of blood vessels makes the tissue within the AZ more elastic and malleable than the surrounding vascularized retina. Models evaluated the contribution to pit formation of varying elasticity ratios between the AZ and surrounding retina, AZ shape, and width. The separate and interactive effects of two mechanical variables, intraocular pressure (IOP) and ocular growth-induced retinal stretch, on pit formation were also evaluated. Either stretch or IOP alone produced a pit when applied to a FEA model having a highly elastic AZ surrounded by a less elastic region. Pit depth and width increased when the elasticity ratio increased, but a pit could not be generated in models lacking differential elasticity. IOP alone produced a deeper pit than did stretch alone and the deepest pit resulted from the combined effects of IOP and stretch. These models predict that the pit in the AHA is formed because an absence of vasculature makes the inner retinal tissue of the AZ very deformable. Once a differential elasticity gradient is established, pit formation can be driven by either IOP or ocular growth-induced retinal stretch.

Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation.

By establishing an avascular, highly elastic, region within the fetal area of high acuity (AHA), the developing primate eye has created a unique substrate on which the mechanical forces of intraocular pressure (IOP) and growth-induced retinal stretch (stretch) can act. We proposed (Springer & Hendrickson, 2004b) that these forces generate both the pit and high cone density found in the adult AHA. In this paper, we use quantitative measures to determine the temporal relationships between nasal and temporal retinal elongation, changes in pit depth, cone packing, and cone morphology over M. nemestrina retinal development. Retinal length increased rapidly to about 105 days postconception (dpc; Phase 1) and then elongation virtually ceased (Phase 2) until just after birth (180 dpc). Retinal elongation due to stretch resumed during Phase 3 until approximately 315 dpc (4–5 months), after which time the retina appeared mature (Phase 4). The pit appeared during the quiescent Phase 2, suggesting that IOP acts, in conjunction with molecular changes in the inner retina, on the highly elastic, avascular, AHA to generate a deep, narrow pit and causes inner retinal cellular displacements. Subsequently (Phase 3), the pit widened, became 50% shallower and central inner retinal lamina thinned slightly due to a small amount of retinal stretch occurring in the AHA. Centripetal movement of cones was minimal until just after birth when the pit reached 88% of its maximal depth. Accelerated cone packing during Phase 3 was temporally correlated with increased stretch. A slight stretching of the central inner retina generates “lift” forces that cause the pit to become shallower and wider. In turn, these “lift” forces draw cones toward the center of the AHA (Springer, 1999). Localized changes in cone morphology associated with packing, included smaller cell body size, a change from a monolayer to a multilayered mound of cell bodies, elongation of inner segments and tilting of the apical portion toward the AHA. These changes began in cones overlying the edges of the pit, not its center. Henle cone axons formed initially in association with centrifugal displacement of the inner retina during pit formation, with an additional subsequent elongation due to cones moving centripetally. An integrated, two-factor model of AHA formation is presented. Initially, during the second half of gestation (Phase 2), IOP acts on the hyperelastic avascular zone of the AHA to generate a deep pit in the inner retina. In the first 4 months after birth (Phase 3), central retinal stretch generates tensile “lift” forces that remodel the pit and pack cones by drawing them toward the AHA center.

https://www.cambridge.org/core/services/aop-cambridge-core/content/view/9E194D87908003047489313535FBEA6F/S095252380522206Xa.pdf/div-class-title-development-of-the-primate-area-of-high-acuity-3-temporal-relationships-between-pit-formation-retinal-elongation-and-cone-packing-div.pdf

Development of the primate area of high acuity, 3: temporal relationships between pit formation, retinal elongation and cone packing.

Mechanisms underlying the development of the primate area of high acuity (AHA) remain poorly understood. Finite-element models have identified retinal stretch and intraocular pressure (IOP) as possible mechanical forces that can form a pit (Springer & Hendrickson, 2004). A series of Macaca nemestrina monkey retinas between 68 days postconception (dpc) and adult were used to quantify growth and morphological changes. Retinal and pars plana length, optic disc diameter, disc-pit distance, and inner and outer retinal laminar thickness were measured over development to identify when and where IOP or stretch might operate. Horizontal optic disc diameter increased 500 mum between 115 dpc and 2 months after birth when it reached adult diameter. Disc growth mainly influences the immediate surrounding retina, presumably displacing retinal tissue centrifugally. Pars plana elongation also began at 115 dpc and continued steadily to 3-4 years postnatal, so its influence would be relatively constant over retinal development. Unexpectedly, horizontal retinal length showed nonlinear growth, divided into distinct phases. Retinal length increased rapidly until 115 dpc and then remained unchanged (quiescent phase) between 115-180 dpc. After birth, the retina grew rapidly for 3 months and then very slowly into adulthood. The onset of pit development overlapped the late fetal quiescent phase, suggesting that the major mechanical factor initiating pit formation is IOP, not retinal growth-induced stretch. Developmental changes in the thickness of retinal layers were different for inner and outer retina at many, but not all, of the ten eccentricities examined.

Alan D. Springer

Papers

Centrifugal innervation of goldfish retina from ganglion cells of the nervus terminalis

Retinal projections in the goldfish: A study using cobaltous‐lysine

Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation.

Development of the primate area of high acuity, 3: temporal relationships between pit formation, retinal elongation and cone packing.

Development of the primate area of high acuity. 2. Quantitative morphological changes associated with retinal and pars plana growth.