Fig. 1. Lateral diagrammatic view of the accessory optic tract. The accessory fibers do not appear to run in a single bundle in the optic chiasma and tract as might be assumed from the diagram but are interspersed with other fibers
By Elwin Marg, Berkeley, California (USA)
Introduction
The accessory optic system is a visuosensory pathway with a direct retinal input to the midbrain. It is perhaps less known than the other three optic systems originating in the retina: (1) the primary visual system to the lateral geniculate bodies, (2) the retinopretectal system, and (3) the retinotectal system. All optic axons from the contralateral retina which do not terminate in the lateral geniculate bodies, pretectal nuclei or tectum constitute the definitive accessory optic system.
Early histological inquiry into the cellular organization and the fiber connections of the accessory optic system was initiated nearly a century ago, and historical reviews of this subject are to be found elsewhere (HAMASAKI and MARG, 1960; HAYHOW, 1959, 1966; HAYHOW et al., 1960; GIOLLI, 1961, 1963; and GIOLLI et al., 1968). Physiological investigations of the accessory optic system have been made only recently with functional data being reported first by MARG et al. (1959) and subsequently by HAMASAKI and MARG (1960, 1962), HILL and MARG (1963), WALLEY (1967) and PASIK and PASIK (1965, 1966, 1968).
Anatomy
The accessory optic system provides a primary or direct retinal input to themidbrain tegmentum, and specifically to the nucleus of the transpeduncular tract (GIOLLI et al., 1968). accessory optic system with either anterior and/or posterior accessory optic tracts appears to characterize every class of vertebrates. This system has been described in a wide series of vertebrates and found to consist of from one to three pairs of fiber fasciculi. Hence in birds, reptiles and amphibians, one pair of fasciculi have been revealed and designated as the "basal optic roots". Among mammals, the accessory optic system reaches its anatomic zenith with 2 - 3 pairs of well-developed bundles in Rodentia (HAYHOW et al., 1960), Lagomorpha (GIOLLI, 1961) and Tupaia (TIGGES, 1966; CAMPBELL et al., 1967) but is seen in a state of degeneracy with only one pair of small, fore-shortened tracts in prosimians (CAMPOS-ORTEGA and CLUVER, 1968; TIGGES and TIGGES, 1968, 1969) and simians (GIOLLI, 1963; HASSLER, 1965; CAMPOS-ORTEGA and GLEES, 1967).
In the monkey the accessory optic system appears to be capable of performing a basic visuosensory function when the striate cortex is destroyed (PASIK and PASIK, 1965, 1966, 1968, 1972). In the intact animal, the accessory optic system provides a direct visual pathway to the midbrain tegmentum although its normal function (if indeed it has one) remains to be determined (MARG, 1964).
History
The literature related to the accessory optic system goes back to GUDDEN who in 1870 described a tract passing across the cerebral peduncle and appropriately named it the tractus peduncularis transversus. In a subsequent paper GUDDEN (1881) convincingly demonstrates that the tract, which is included as part of the optic nerve and optic chiasma, depended on the intact retina. Removal of the retina would cause its subsequent degeneration. Shortly after, BECHTEREW (1894) describes its nucleus of termination, the nucleus of the tractus peduncularis transversus, as lying between the red nucleus and the substantia nigra.
With the discovery of the anterior accessory optic tract by BOCHENEK in 1908, a new pathway was added to the accessory optic system. It goes as part of the optic nerve and optic chiasma, passing through the cerebral peduncle and terminates in the nucleus of the tractus peduncularis transversus (GIOLLI, 1961; HAYHOW, 1966). The original "tractus peduncularis transversus" described by GUDDEN is also designated the posterior accessory optic tract to distinguish it from the more anterior bundle of BOCHENEK. For reviews on the experimentation pertaining to the accessory optic pathways, the reader is referred to: HAYHOW (1959), HAMASAKI and MARG (1960), GIOLLI (1963), and MARG (1964).
Stereotaxic Recording and Stimulation
As in the primary visual system, the neurophysiology of the accessory optic system-can be studied directly with the aid of electrodes in experimental animals. The only additional special problem arises from the minuteness of the accessory optic structures. For example, the nucleus of the tractus peduncularis transversus (anglicised name: nucleus of the transpeduncular tract) occupies about one square mm of projected area deep in the brain. When the structure is pierced from the top surface of the brain with an electrode tip, one cannot help be exalted by the feeling that it is a {eat of stereotaxic marksmanship. Of course the "bull's eye" is subject to conclusive histological confirmation but the target can be recognized immediately by the response to light stimulation of the contralateral retina or electrical stimulation of the contralateral optic nerve. An evoked potential can be recorded from the nucleus of the transpeduncular tract (NTPT). If now the NTPT is electrically stimulated, no response can be obtained antidromically from the contralateral optic nerve, forcing the conclusion that the pathway is polarized. There must be a synaptic station between the NTPT and the optic nerve which allows only centripetal flow of neural impulses. The pathway is divided into two parts and to clarify its nomenclature: (i) the proximal part can be called the posterior accessory optic tract and (ii) the distal part the transpeduncular tract (consult Fig. l). Each tract terminates within its respective nucleus.
Fig. 1. Lateral diagrammatic view of
the accessory optic tract. The accessory fibers do not
appear to run in a single bundle in the optic chiasma and tract
as might be assumed from the diagram but are interspersed with
other fibers
Organization of Pathways
As mentioned previously, the anterior accessory optic tract terminates in the nucleus of the transpeduncular tract. It is plain from Fig. 1 that an antidromic response would be recorded at the optic nerve from electrical stimulation of the nucleus of the transpeduncular tract if the pathway were direct and were functional. Yet there is no histological evidence of a synaptic interruption (as indeed there appears to be none in the posterior accessory optic tract of the rabbit but clearly one in the monkey). Furthermore the antidromic signal is not passed. There seems no choice but to disregard this pathway functionally in the context of current knowledge, despite its established morphology.
There is additional neurophysiological evidence of a cell station in the optic pathway to the nucleus of the transpeduncular tract. This includes the effect of post-tetanic potentiation, effects of asphyxia on synaptic transmission and the maximum frequency limitation of the response of a synaptic pathway. Direct comparison using these criteria of the accessory pathway with a part of the primary visual pathway known to have direct fibers without a cell station points to the synapse in the accessory pathway.
Response Characteristics
Curiously, the light response recorded at the nucleus of the transpeduncular tract is mainly "on". Unit recording shows primarily "on" units, some "on-off" with the "on" moiety predominating, and uncommonly an "off" unit. Unlike in the primary visual pathway, single units do not respond uniformly to flicker stimulation of the retina. The neurons cease responding in a frequency band from a few to 10 or 15 Hz, but the response is faithful at both lower and at higher frequencies.
Some cells in the nucleus of the transpeduncular tract show different maximal response depending upon the wavelength of the light stimulus. The nucleus, however, exhibits less hue information than does the dorsal lateral geniculate nucleus. The nucleus would be consequently of limited concern in a possible color vision system (HILL and MARG, 1963).
The receptive fields of the cells in the nucleus of the transpeduncular tract are extremely large, some having diameters up to 90 degrees (WALLEY, 1967). More than half the units recorded are directionally selective to vertically moving stimuli. Most of them yield greater responses to upward rather than downward movement. The detection of vertical movement could be related to visual orientation and the detection of predators.
Indwelling electrodes in the rabbit nucleus of the transpeduncular tract allow its electrical stimulation in the unanesthetized and unrestrained animal. The response of the rabbit appears identical to similar stimulation of other sites in the midbrain and adjacent areas. The picture is typical of arousal from stimulation of the mesencephalic reticular formation (MARG and GIOLLI, unpublished observations, 1962; MARG, 1964).
Monkey and Rabbit
GIOLLI (1963) has demonstrated a structural organization of the accessory optic system of the Cynomolgus monkey which is in virtual agreement with the functional concept derived from physiological experimentation on the rabbit (Fig. 2). He describes a foreshortened transpeduncular tract (his accessory optic tract). This tract ends within GIOLLI'S accessory optic nucleus rather than in the nucleus of the transpeduncular tract as classically described in non-primate mammals. The fine structure and synaptic organization are described by PASIK et al. (1970, 1971). They have found that the system has uncrossed as well as crossed elements. The stretch of transpeduncular tract consists of non-accessory optic axons which probably originate in the accessory optic nucleus and innervate the nucleus of the transpeduncular tract (GIOLLI, 1963). Physiological studies by HAMASAKI and MARG (15360, 1962) support the view that the homolog of GIOLLIS accessory optic nucleus in the rabbit represents a synaptic station between the retina and the nucleus of the transpeduncular tract.
Electrophysiological investigation of the monkey is desirable to compliment histological data. It is complicated at least in the Cynomolgus monkey, by the imprecision of laboratory stereotaxic methods as the loci of various structures of the simian brain arc not well correlated with the loci of bony landmarks on the skull. Techniques developed for human stereotaxic surgery could be used to overcome this problem, using X-ray localization of landmarks within the brain itself. But its relatively high cost combined with the equally high cost of monkeys is a deterrent.
Fig. 2. Lateral diagrammatic view of
the accessory optic system in the monkey. This diagram is
also in accord with the neurophysiological results in the rabbit
Visual Function
A number of investigators have shown that animals with their striate cortex removed have some residual visual function (KLUVER, 1942; DOTY, 1961; PASIK et al., 1961; SNYDER et al., 1966; SCHILDER, 1966; SPRAGUE, 1966; WINANS, 1967; COOPER et al., 1967; PASIK and SCHILDER, 1967). Recently PASIK and PASIK (1965,1966,1968,1970,1972) removed the striate cortex from monkeys in an attempt to find the afferent pathway for this residual vision. Further experimentation and the systematic elimination of possible structures (prestriate and temporal neocortices, nucleus pulvinaris posterior, superior colliculi, medial and lateral pretectum) made it evident that the lateral region of the midbrain diencephalon junction is critical for the residual vision. This area appears to receive input through the accessory optic system since all monkeys that failed a light discrimination test had either destruction or retrograde degeneration of the accessory optic nucleus. The accessory optic system appears to be necessary for the basic discrimination of total luminous flux in the absence of striate cortex.
Obviously the limited number of fibers in the system would not support good visual acuity, nor would, it seems, a termination in the midbrain reticular formation and substantia nigra (GIOLLI et al., 1968) rather than in the visual cortex. Furthermore, KOSTOVIC (1971)) has demonstrated in the rat that there is no retinal topographical organization of the fibers terminating in the nucleus of the transpeduncular tract. But the ability to utilize visual information as demonstrated behaviorly through the accessory optic system makes one consider how few neurons arc necessary and further that access of this information to the brain need not necessarily be at the cortical or even the thalamic level of the brain.
Some investigators (SCHNEIDER, 1967; INGLE, 1967; HELD, 1968; TREVARTHEN, 1968) have divided the visual system into two parts based on the processing of information: one cortical for discrimination, evaluation, analysis, shape or focal vision and the other collicular for localization, orientation, position or ambient vision. Morphologically, however, there are at least four visual systems which originate in the retina. In addition to the geniculo-cortical system and the tectal system, there is not only the accessory optic system but also the pretectal system concerned with pupillomotor functions. If one is not limited to direct retinal origin, more systems can be invoked such as the inferotemporal cortical visual system (see chapter by C. GROSS). Divisions which correlate function with structure arc, of course, valuable steps in our analysis and understanding of systems.
MAEKAWA and SIMPSON(1972) find that the accessory optic system in rabbits is a visual pathway to the flocculus of the cerebellum. Activation of that pathway produces a response in the climbing fibers which is ipsilateral to the stimulated eye.
Fig. 3. Single units recorded from the
nucleus of the transpeduncular tract responding to photic
stimulation of the contralateral eye. a and b On
response, c and d On-off response. Note that
the on response is greater than the off
Possible Retino-Hypothalamic Pathway
Although not a part of the accessory optic system per se, any possible direct retino-hypothalamic pathway is of parallel interest. Neurohistologists have searched for fibers fitting this description while studying the accessory optic system. Physiologically, FELDMAN (1964), on the basis of strong, short latency, visually evoked potentials in the anterior hypothalamus and preoptic areas of the cat, concluded that direct innervation existed. Some anatomical evidence supports the direct pathway (KNOCHE, 1957;SOUSA-PINTO, 1970;SOUSA-PINTO and CASTRO-CORREIA, 1970) but there is much negative evidence also (GIOLLI and GUTHRIE, 1969; HAYHOW et al., 1960; KIERNAN, 1967).
Other Functions
Some recent investigations have implicated the accessory optic system in non-visual systems of the brain. It may be the afferent pathway in light-controlled endocrine mechanisms (CRITCHLOW, 1958: THOMPSON et al., 1964: MOORE et al., 1967) and may be responsible for the pineal response to light in the monkey (MOORE, 1969). Additionally, the termination of the supraoptic decussations (of Ganser, Gudden, anti Meynert) have been associated with the nucleus ofthe posterior accessory optic tract (MINDERHOUT, 1967).
A discussion of possible functions of the accessory optic system has beenpresented (MARG, 1964). It does not seem that the system transmits a spatial image because of a paucity of fibers relative to the primary visual pathway. An alerting-arousal function is supported as would be expected from the anatomical location but no oculomotor function was noted. Postural information could be oneof its functions. Evidence for its possible role in circadian rhythms is lacking The nucleus of the transpeduncular tract appears to have no centrifugal-retinal function while this potential function for the accessory optic nucleus has not been investigated.
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