Intermediate constructs are required as bridges between complex behaviors and realistic models of neural circuitry. For cognitive scientists in general, schemas are the appropriate functional units; brain theorists can work with neural layers as units intermediate between structures subserving schemas and small neural circuits.

After an account of different levels of analysis, we describe visuomotor coordination in terms of perceptual schemas and motor schemas. The interest of schemas to cognitive science in general is illustrated with the example of perceptual schemas in high-level vision and motor schemas in the control of dextrous hands.

Rana computatrix, the computational frog, is introduced to show how one constructs an evolving set of model families to mediate flexible cooperation between theory and experiment. Rana computatrix may be able to do for the study of the organizational principles of neural circuitry what Aplysia has done for the study of subcellular mechanisms of learning. Approach, avoidance, and detour behavior in frogs and toads are analyzed in terms of interacting schemas. Facilitation and prey recognition are implemented as tectal-pretectal interactions, with the tectum modeled by an array of tectal columns. We show how layered neural computation enters into models of stereopsis and how depth schemas may involve the interaction of accommodation and binocular cues in anurans.

An avian retinopetal nucleus, the isthmo-optic nucleus (ION), is known to receive predominant inputs from the ipsilateral optic tectum. We injected biocytin into the ION in the Japanese quail, and retrogradely labeled tectal neurons projecting to the isthmo-optic (IO) neurons, or the tecto-IO neurons, with an extraordinary Golgi-like quality. Somata of the tecto-IO neurons were located in layer 9 of the tectum. The tecto-IO neurons did not have apical dendrites extending into superficial retino-recipient layers (layers 2–7), but had descending dendrites ramified in layers 9–12. They also possessed short ascending dendrites ramifying in the upper half of layer 9. This dendritic morphology suggests that main input to the tecto-IO neurons may not be of retinal origin. The tecto-IO neurons were spatially arranged in a regular pattern. Distances between neighboring tecto-IO neurons were 50–100 μm. The dendrites of each tecto-IO neuron were not widely dispersed in the horizontal plane, and were confined in a vertically oriented column of 100–200 μm diameter. They possessed axon collaterals extending horizontally in layers 12 and 13. The estimated total number of the tecto-IO neurons was approximately 7000–10,000, which is almost identical to the total cell number of the IO neurons. To label a small number of the tecto-IO terminals, biocytin was injected into a confined area of the optic tectum. The tecto-IO fibers densely arborized in a restricted space of the ION, which is comparable to the dimension of dendritic arborization of individual IO neurons. It is suggested that single tecto-IO neurons may make contact with single IO neurons. IO neurons are known to make synaptic contact with single target cells (association cells of Cajal) in the retina (Uchiyama & Ito, 1993; Uchiyama et al., 1995). The arborization pattern of the tecto-IO neurons' dendrites indicates that the tecto-IO neurons receive very local information in sensory and sensorimotor coordinate space. The morphology of the tecto-IO terminals suggests that the spatially confined information that drives the tecto-IO neurons is sent in parallel to single IO neurons, and then further to single retinal association cells of Cajal. Cellular-level restricted projection patterns of the tecto-isthmo-retinal system may reflect its function for centrifugal control of retinal function.

In the frog Xenopus laevis, the isthmotectal projection, which relays input from the ipsilateral eye, exhibits anatomical reorganization following surgical eye rotation performed during tadpole stages while the isthmotectal projection in the frog Rana pipiens fails to show reorganization. This plasticity has been shown to be dependent upon activation of the N-methyl-D-aspartate (NMDA) receptor located on tectal cell dendrites. The reorganization process in Xenopus is hypothesized to employ a Hebbian mechanism requiring correlated firing of ipsilateral and contralateral inputs to a given tectal cell; when an ipsilateral axon synapses onto a tectal cell that receives input from a contralateral axon with a matching receptive-field location, the correlation in activity triggers stabilization of the ipsilateral synapse. However, in neither Xenopus nor Rana do ipsilateral and contralateral inputs begin to fire simultaneously in response to a given visual stimulus; the ipsilateral input is delayed because it reaches the tectum indirectly, through a polysynaptic relay via the opposite tectum and nucleus isthmi. The objective of this experiment was to test whether there is a significant difference in this intertectal delay between Xenopus laevis and Rana pipiens in order to determine whether intertectal delay could be a contributing factor in this species-specific ability to exhibit visual plasticity. We have found that intertectal delay is 26.16 ms longer in Rana pipiens (36.53 ms) than in Xenopus laevis (10.37 ms).

Previous biochemical and immunohistochemical studies have shown that the neurotensin-related hexapeptide LANT6 is widespread and abundant in the avian nervous system. In the present study, immunohistochemical techniques were used to show that LANT6 is present in numerous cells of the retinal ganglion cell layer in pigeons. Consistent with the possibility that these LANT6+ retinal cells might be retinal ganglion cells, it was found that (1) the distribution of LANT6+ fibers and terminals in the central retinal target areas matched the distribution of central retinal projections; (2) the LANT6+ fibers and terminals are eliminated from retinal target areas by transection of the contralateral optic nerve; and (3) LANT6+ retinal cells in the ganglion cell layer can be retrogradely labeled by injections of fluorogold in the tectum. These results suggest that LANT6 may be utilized as a neuroactive substance by the central terminals of numerous retinal ganglion cells in birds. Similar anatomical findings have been previously reported for members of several other vertebrate groups, giving rise to the possibility that LANT6 (or its homologues in nonavians) may be a phylogenetically ubiquitous neuroactive substance used by retinal ganglion cells.

Like many diurnal raptors, the American kestrel or sparrow hawk, Falco sparverius, possesses two foveae in each eye. In this study, we used fundus photography and reversed ophthalmoscopy to plot the projection of these foveae onto the visual field, together with other retinal landmarks such as the pecten and ora terminali. From such data, it was determined that the central monocular fovea (CMF) and temporal binocular fovea (TBF) were separated by 36 deg and that the kestrel has 58 deg of binocular overlap when the eyes are appropriately converged. Single-cell and multi-unit recordings were used to systematically explore the tectal surface and map receptive fields (RF) onto a hemispheric screen. A retinotopic map of the tectal surface was produced from such data and revealed an expanded representation for each fovea on the tectum and a systematic increase in RF size from fovea to periphery. The functional significance of this organization is discussed.

Connections of the rabbit suprageniculate pretectal nucleus (SP) with the superior colliculus were explored by means of retrograde transport of horseradish peroxidase or Fluorogold. Large injections centered in the superficial and intermediate tectal layers resulted in bilateral retrograde transport to the medium-size multipolar neurons of the suprageniculate pretectal nucleus. Horseradish peroxidase was also transported anterogradely into the ipsilateral and contralateral neuropiles of the suprageniculate pretectal nucleus. The labeled cells in SP were dispersed throughout the nucleus, including its dorsal, wedge-shaped, internal portion. Labeling was mainly ipsilateral, and less abundant on the contralateral side.

The superior colliculus exerts its most direct influence over orienting movements, and saccades in particular, via its descending projections to the brain stem and spinal cord. However, while there is detailed physiological data concerning the generation of saccade-related activity in the primate superior colliculus, there is relatively little data on the detailed connectivity of this structure in primates. Consequently, retrograde transport techniques were utilized to determine the locations of the cells of origin of these descending pathways in macaque monkeys. Tectal cells that projected to the ipsilateral pontine reticular formation were mainly found in the deep gray layer and occasionally in the intermediate gray layer. Tectal cells that projected to the contralateral pontine reticular formation were predominantly located in the intermediate gray layer. The contralaterally projecting population could be subdivided into two groups. The cells in upper sublamina of the intermediate gray layer project primarily to the saccade-related regions of the paramedian reticular formation. Cells in the lower sublamina project primarily to more lateral regions of the pontine reticular formation and to the spinal cord. We conclude that the primate colliculus is provided with at least three descending output channels, which are likely to differ in their connections and functions. Specifically, it seems likely that the lower portion of the intermediate gray layer may be specialized to subserve combined head and eye orienting movements, while the upper sublamina subserves saccades.

Immunocytochemical techniques have been used to examine the distribution of substance-P (SP)-labeled neurons in the superior colliculus of rats from birth to adulthood. At birth, there are almost no SP-immunopositive neurons in the tectum. A small number of SP neurons appear over the next several days. However, the vast majority of SP neurons appear between P9 and P10, and by P12 have attained adult-like numbers and distribution. Neurons are confined to the superficial layers of the colliculus, specifically the upper two-thirds of the stratum griseum superficiale (SGS). There is no indication of a differential developmental sequence along rostrocaudal or mediolateral axes. Neuronal types can be distinguished as early as P6 and include horizontal, vertical, and multipolar cells.

Substance-P-immunoreactive axons and boutons are also present in the superior colliculus at birth, and are for the most part confined to the deep layers. Boutons are generally of the en-passant type. The density of labeled axons and boutons increases progressively, and by P10 there is an almost adult-like lamination and patchiness. In the adult, labeled axons and boutons are most dense in the stratum opticum and stratum griseum intermedium. Bridges of dorsoventrally oriented labeled axons span the relatively label-poor stratum album intermedium. SP label in the stratum griseum profundum is dense and patchy, and there is also dense label in the stratum album profundum bordering the periaqueductal grey.

The role of substance-P-labeled neurons in the superior colliculus is still a matter of speculation. The findings of this study indicate that SP neurons may play a role in intrinsic collicular circuitry.

To investigate the circuitry that mediates binocular interactions in the tectum of Xenopus frogs, we have begun to identify the tectal cells that receive ipsilateral eye input relayed via the nucleus isthmi. Isthmotectal axons were labeled with horseradish peroxidase, and thin sections were labeled by postembedding immunogold reaction with antibodies to γ-aminobutyric acid (GABA). Ultrastructural examination reveals that many isthmotectal axons terminate on GABA-immunoreactive dendrites. Other isthmotectal axons contact postsynaptic structures that are unlabeled but have an appearance consistent with previously described GABA-poor zones of GABA-immunoreactive dendrites. We also examined the unlabeled inputs to the dendrites that were postsynaptic to filled isthmotectal axons. The most common nonisthmic inputs to those dendrites were GABA-immunoreactive processes with symmetric morphology. Surprisingly, we found only one input with the retinotectal characteristics of densely packed round, clear vesicles and minimal GABA immunoreactivity. These results indicate that isthmotectal axons synapse onto inhibitory interneurons, that retinotectal and isthmotectal axons do not synapse close to each other on the same dendrites, and that inhibitory connections are the closest neighbors to isthmotectal synapses.

Contrary to the traditional view that receptive fields are limited in spatial extent, recent studies have indicated that the response of neurons to a local stimulus within the receptive field can be modulated by stimulation of the surrounding region. Here we quantified the nature of these contextual effects on visual motion responses of neurons in the pigeon's optic tectum using standard extracellular recording techniques. All of the cells tested responded well to a test spot moving across their receptive fields. When a background pattern was moved in the same or in a similar direction as that of the test spot, the responses of most deep tectal neurons to the test spot were maximally inhibited. Movement of the background in the opposite or near opposite direction produced minimal inhibition or even facilitation. For some deep tectal neurons, this directionally selective modulation by the moving background was maintained when the background motion was paired with different movement directions of the test spot (including both the preferred and least preferred directions). Thus, this selectivity for opposing motion was independent of the absolute direction of either the test spot or the background, a finding which is consistent with the results reported by Frost and Nakayama (1983), although they did not include all test spot directions. For some other neurons, identified here for the first time, the background movement selectively modulated the response only when the test spot moved in the neuron's preferred directions. These neurons lost selectivity for opposing motion when the test spot moved in nonpreferred directions. The significance of these contextual effects on the motion response of tectal neurons may be related to how the brain distinguishes self-induced motion from object motion and segregates figure from ground.

Retinal and visual function returns following retinal destruction by ouabain in adult goldfish (Carassius auratus). Although the precise cellular mechanisms are unclear, the ability to regenerate CNS neurons and connections that subsequently sustain visual behavior is remarkable, especially for an adult vertebrate. In this paper, we ask whether visual stimulation via new retinal cells can activate existing cells in the optic tectum, which normally receives the largest retinal projection in this species. The right eyes of adult goldfish were injected with ouabain. After 1–18 weeks the conscious, freely moving fish were exposed to spatially and temporally varying visual stimuli and the resulting tectal metabolic activity was determined with the autoradiographic deoxyglucose method. In normal controls without lesions, visual stimulation produced equally strong metabolic activity in both tectal hemispheres, peaking in the layer where most retinotectal projections terminate (N = 6). One week after ouabain injection, metabolic activity in the contralateral, deprived tectum was dramatically reduced (N = 5), closely resembling the effect of unilateral ocular enucleation (N = 5). However, 9–18 weeks after ouabain injection, metabolic activity in the deprived tectum recovered to a level that was statistically indistinguishable from normal controls (N = 6). These findings suggest that, after a comprehensive cytotoxic lesion of the retina, regenerated ganglion cells not only establish new connections with the preexisting optic tectum, but also effectively transmit visual information they receive from newly generated photoreceptors to the “old” tectum.

Nitric oxide (NO) is a neuronal messenger molecule that mediates pathway refinement in some brain regions. We used nicotinamide adenine dinucleotide phosphate diaphorase (NADPHd) histochemistry to examine the development of NO expression in the superior colliculus (SC) of kittens aged E28–E58 and P2–P57 and adults in order to determine if NO expression is correlated with pathway refinement. At E28, labeled cells were seen only within the subventricular zone (SVZ). At E36–E41, labeled cells were also found within the deep gray layer (DGL) of SC. At E51 and E58, a few labeled neurons were also present in the intermediate gray layer (IGL). These neurons already had extensive dendritic fields and well-developed morphologies at the time that they first expressed nitric oxide synthase (NOS). The number of neurons labeled in the DGL and IGL increased postnatally, reaching a peak density between P14 and P35. Neurons within the optic (OL) and superficial gray layers (SGL) were first visible at P7 and increased slightly in number until adulthood. However, SGL-labeled neurons were relatively limited in number and lightly labeled at all ages examined. We conclude that (1) NADPHd expression occurs in SC beginning in the second trimester in kittens and progresses in a ventral to dorsal pattern between E36–P35; (2) few neurons in kitten SGL are labeled by NADPHd and these appear relatively late in postnatal development; and (3) there is no correlation between NOS expression and retinocollicular pathway refinement in kittens, a result different from that seen in rodents.

In the rat, the superficial gray layer (SGS) of the superior colliculus receives glutamatergic projections from the contralateral retina and from the visual cortex. A few fibers from the ipsilateral retina also directly innervate the SGS, but most of the ipsilateral visual input is provided by cholinergic afferents from the opposing parabigeminal nucleus (PBG). Thus, visual input carried by cholinergic afferents may have a functional influence on the responses of SGS neurones. When single neuronal extracellular recording and iontophoretic drug application were employed to examine this possibility, cholinergic agonists were found to depress responses to visual stimulation. Lobeline and 1-acetyl-4-methylpiperazine both depressed visually evoked activity and had a tendency to reduce the background firing rate of the neurones. Carbachol depressed the visual responses without any significant effect on the ongoing activity, while the muscarinic receptor selective agonist methacholine increased the background activity of the neurones and reduced their visual responses. Lobeline was chosen for further studies on the role of nicotinic receptors in SGS. Given that nicotinic receptors are associated with retinal terminals in SGS, and that the activation of presynaptic nicotinic receptors normally facilitates transmitter release (in this case glutamate release), the depressant effects of nicotinic agonists are intriguing. However, many retinal afferents contact inhibitory neurones in SGS; thus it is possible that the increase in glutamate release in turn facilitates the liberation of GABA which goes on to inhibit the visual responses. We therefore attempted to reverse the effects of lobeline with GABA receptor antagonists. The depressant effects of lobeline on the visual response could not be reversed by the GABAA antagonist bicuculline, but the GABAB antagonist CGP 35348 reduced the effects of lobeline. We hypothesize that cholinergic drive from the parabigeminal nucleus may activate presynaptic nicotinic receptors on retinal terminals, thereby facilitating the release of glutamate onto inhibitory neurones. Consequently GABA is released, activating GABAB receptors, and thus the ultimate effect of nicotinic receptor activation is to depress visual responses.

Immunohistochemistry for choline acetyltransferase (ChAT) revealed an extensive network of cholinergic fibers in the tectum of amphibians. The distribution of ChAT immunoreactive fibers was not restricted to superficial retinocipient layers, but also included deep tectal layers. The aim of the present study was to investigate the origin of the cholinergic inputs to the tectum of amphibians. For that purpose, application of retrograde tracers in the tectum of the anuran Rana perezi and the urodele Pleurodeles waltl was combined with ChAT immunohistochemistry. Double-labeled cells were found primarily in the nucleus isthmi of both species. The cholinergic isthmotectal projection is bilateral and topographically arranged and all retrogradely labeled cells found in this nucleus were ChAT immunoreactive. Remarkably, abundant cholinergic cells in two tegmental nuclei, the pedunculopontine tegmental nucleus (anurans) and the laterodorsal tegmental nucleus (anurans and urodeles), were demonstrated to provide additional cholinergic innervation to the tectum. We compare the present results with previously reported studies in amphibians and other vertebrates, and discuss the possible functional significance of the cholinergic innervation of the amphibian tectum.

Birds have a well-developed centrifugal pathway from the isthmo-optic nucleus to the retina. In the present study, receptive-field properties of the isthmo-optic (IO) neurons and suppressive effect of remote stimuli far beyond the “classical” receptive fields were examined electrophysiologically in the Japanese quail. Receptive fields emitting more than half the maximal ON–OFF response to a small spot of light measured 4.3 ± 1.9 deg (n = 37) in diameter. A stationary spot of light was presented at a remote point (35–76 deg) away from the receptive-field center, besides a stimulus for the receptive-field center, with various onset time difference. The peripheral spot, when turned on 50–100 ms before the center spot, maximally suppressed the ON and OFF responses to the center spot. In most of the IO neurons examined (13 out of 15 units), even small remote stimuli (2–5 deg in diameter) significantly suppressed the ON–OFF responses to the center stimulus. The suppressive effects of remote stimuli were seen to be extended to, at least, two thirds of the entire visual field of a single eye. Such wide suppressive fields indicate that the IO neurons may compete with each other for activity in a very long-range scale. Simulation using a simple static model based on three basic principles of processing of the centrifugal visual system— topographical input, long-range competition, and local gain enhancement—suggests that the system could function as an autonomous mechanism for attentional object selection.