Visual shape discrimination in goldfish, modelled with the neural circuitry of optic tectum and torus longitudinalis.

There is no satisfactory neurally-based theory as to how vertebrates that lack a neocortex discriminate even simple geometric shapes. In fishes, an intact optic tectum is necessary for such discriminations, but physiological studies of it have found nothing like the hierarchically arranged feature detecting neurons of mammalian visual cortex. Here, a neural model attempts a solution by basing shape discrimination upon the responses of only those elementary detectors (e.g. of size) that are within a focus of attention, formed by a winner-take-all arrangement of retinotopically mapped units representing tectal pyramidal cells. While this relatively primitive mechanism could recognize an object irrespective of position in space, it fails to distinguish patterns that differ only in their features' spatial relationships. The model's solution - imitating goldfish that naturally attend to the top of shapes - is to shift attention to the edges of a shape by spatially offsetting inputs to the pyramidal neurons, effected by the torus longitudinalis and its prolific synapses on pyramidal dendrites. The model's shape discrimination was compared to an extensive behavioral study using shapes with points and projections. In one test series fish were sensitive to the relative number of points on the tops of shapes. In another, fish were trained to discriminate points on the sides. By using different offset connections and only one elementary feature detector for small dark spots, the model successfully emulated the two sets of goldfish data, as judged by significant correlations between model response and fish discrimination.

Acuity and contrast sensitivity of the bluegill sunfish and how they change during optic nerve regeneration.

Spatial vision was studied in the bluegill sunfish, Lepomis macrochirus (9.5-14 cm standard length) to assess the limitations imposed by the optics of the eye, the retinal receptor spacing and the retinotectal projection during regeneration. Examination of images formed by the dioptric elements of the eye showed that spatial frequencies up to 29 c/ degrees could be imaged on the retina. Cone spacing was measured in the retina of fresh, intact eyes. The spacing of rows of double cones predicted 3.4 c/degrees as the cutoff spatial frequency; the spacing between rows of single and double cones predicted 6.7 c/degrees. Contrast sensitivity functions were obtained psychophysically in normals and fish with one regenerating optic nerve. Fish were trained to orient to gratings (mean luminance = 25 cd/m2) presented to either eye. In normals, contrast sensitivity functions were similar in shape and bandwidth to those of other species, peaking at 0.4 c/degrees with a minimum contrast threshold of 0.03 and a cutoff at about 5 c/degrees, which was within the range predicted by cone spacing. Given that the optical cutoff frequency exceeds that predicted by cone spacing, it is possible that gratings could be detected by aliasing with the bluegill's regular cone mosaic. However, tests with high contrast gratings up to 15 c/ degrees found no evidence of such detection. After crushing one optic nerve in three trained sunfish, recovery of visual avoidance, dorsal light reflex and orienting to gratings, were monitored over 315 days. At 64-69 days postcrush, responses to gratings reappeared, and within 2-5 days contrast sensitivity at low (0.15 c/degrees) and medium (1.0 c/ degrees) spatial frequencies had returned to normal. At a high spatial frequency (2.93 c/degrees) recovery was much slower, and complete only in one fish.

Sequential recovery of sensitivity to negative and positive contrasts during optic nerve regeneration in goldfish.

A psychophysical procedure, classical conditioning of respiration, was used to measure contrast sensitivity to positive- and negative-contrast discs (8-deg diameter) in goldfish after crushing one optic nerve intraorbitally. In five out of six fish, sensitivity recovered to normal. Recovery times for negative contrasts were significantly shorter than for positive contrasts. The average times postcrush of initial responding to negative and positive contrasts were 23.8 and 30.6 days, and for threshold to come within 0.5 log unit of control values was 29.8 and 39.8 days, respectively. Thereafter, recovery to normal sensitivity was significantly faster for positive contrasts. These results parallel prior observations of neural activity in tectum after optic nerve crush: an early phase of OFF responding followed by a more sudden recovery of ON responding.

Functional properties of retinal ganglion cells during optic nerve regeneration in the goldfish.

After being severed, optic axons in goldfish regenerate and eventually restore the retinotectal map; refinement of the map depends upon impulse activity generated by the ganglion cells. Because little is known about the changes in activity and receptive-field properties of ganglion cells during regeneration, we made extracellular recordings from them in the intact eye up to 95 days after sectioning their axons in the optic tract. Their receptive fields were classified as OFF-, ON-OFF-, or ON-centers, and their axonal conduction velocities measured by antidromic activation. The rate of encountering single units dropped drastically at 4-8 days postsection when only a few OFF-center units could be recorded, recovering to normal between 42 and 63 days. Receptive-field centers were normal in size, except for the few OFF-centers at 4-8 days which were abnormally large. Maintained discharge rates of all types were depressed up to 42 days, but ON-OFF-center units were more spontaneously active than normal around 42 days. Light-evoked responses in OFF-center units were subnormal at 4-8 days, becoming supernormal at 16 days and normal thereafter. ON-OFF- and ON-center units started to regain responsiveness at 16 days, and became supernormal at 42 days, before returning to normal. Conduction velocities of all fiber groups dropped to a minimum at 8 days, the fastest being affected most. There was a gradual recovery to normal conduction velocity by 63 days. The conduction latencies of OFF- and ON-OFF-center units recovered to normal by 42 days, and ON-center units by 63 days. Recovery of ganglion cell responsiveness correlates with functional recovery in the retinotectal system: OFF-center units recover light-evoked responses at about the time OFF activity first reappears in the tectum. ON- and ON-OFF-center units recover later, exhibiting supernormal spiking activity around the time that ON responses reappear in the tectum.

Spectral sensitivity of the goldfish Torus longitudinalis.

We measured the photopic spectral sensitivity of multiunit activity in the torus longitudinalis and optic tectum of goldfish. Since negative contrast stimuli are most effective for exciting torus longitudinalis, spiking activity was evoked by the shadow of a disc moving through a monochromatic light beam projected upon a screen. The amount of activity evoked in torus longitudinalis generally increased with the monochromatic stimulus radiance at the same rate for all wavelengths, indicating a univariant response. Spiking activity in tectum, however, increased at different rates across the spectrum, indicating color-dependent responses. The action spectra for torus longitudinalis were all similar and relatively flat as expected of a homogeneous, broad-band luminance processing system, and about 1 log unit more sensitive than the tectal action spectra. The latter generally displayed sharp peaks and dips in sensitivity indicative of opponent processing.

Axonal conduction velocities of functionally characterized retinal ganglion cells in goldfish.

1. Visual response properties and conduction velocities of retinal ganglion cells were studied by extracellular recordings in the intact goldfish eye. Visually responsive single units were confirmed as ganglion cells by collision testing, and their receptive fields were mapped. 2. From compound action potentials, we identified groups I-V in the optic nerve, with overall conduction velocities of 11.5 +/- 1.17, 7.1 +/- 0.79, 4.4 +/- 0.56, 3.1 +/- 0.31 and 2.3 +/- 0.18 m s-1 (mean +/- S.D.) at 23 degrees C. 3. Ganglion cells were classified by their receptive fields as off-, on-off- or on-centre. Nearly all confirmed ganglion cells had axonal conduction velocities in groups II, III and IV; none fell in the fastest group, I. 4. Off-centre ganglion cells had conduction velocities only in the fast group, II. On-off-centre cells fell mainly in group III, with some in group, II. On-centre cells fell in groups II-V, but mainly in groups III and IV. 5. Receptive field centre diameters were 5-30 deg measured with a photopic background. The mean diameters for off-, on-off- and on-centres were 24, 15 and 18 deg, respectively. The relatively larger diameter and higher rate of spontaneous firing of the off-centre cells were maintained under different adaptation conditions. 6. The off-centre cells can be identified with an anatomical class of large, alpha-like ganglion cells in the goldfish retina.

An analog memory circuit for spiking silicon neurons.

A simple circuit is described that functions as an analog memory whose state and dynamics are directly controlled by pulsatile inputs. The circuit has been incorporated into a silicon neuron with a spatially extensive dendritic tree as a means of controlling the spike firing threshold of an integrate-and-fire soma. Spiking activity generated by the neuron itself and by other units in a network can thereby regulate the neuron's excitability over time periods ranging from milliseconds to many minutes. Experimental results are presented showing applications to temporal edge sharpening, bistable behavior, and a network that learns in the manner of classical conditioning.

Spike train processing by a silicon neuromorph: the role of sublinear summation in dendrites.

A dendritic tree, as part of a silicon neuromorph, was modeled in VLSI as a multibranched, passive cable structure with multiple synaptic sites that either depolarize or hyperpolarize local "membrane patches," thereby raising or lowering the probability of spike generation of an integrate-and-fire "soma." As expected from previous theoretical analyses, contemporaneous synaptic activation at widely separated sites on the artificial tree resulted in near-linear summation, as did neighboring excitatory and inhibitory activations. Activation of synapses of the same type close in time and space produced local saturation of potential, resulting in spike train processing capabilities not possible with linear summation alone. The resulting sublinear synaptic summation, as well as being physiologically plausible, is sufficient for a variety of spike train processing functions. With the appropriate arrangement of synaptic inputs on its dendritic tree, a neuromorph was shown to discriminate input pulse intervals and patterns, pulse train frequencies, and detect correlation between input trains.

The role of torus longitudinalis in equilibrium orientation measured with the dorsal light reflex.

The torus longitudinalis (TL) is a paired elongated structure reciprocally connected with the optic tectum in actinopterygian fishes. Electrophysiological recordings have revealed a sustained neural discharge in TL inversely related to luminance [Northmore, 1984]. This photometric response may play a role in the comparison of light levels between the two eyes, which must occur for the dorsal light reflex (DLR) to orient the body in the environment. Based on the luminance response of TL, it was hypothesized that TL ablation would result in a reduced DLR. Individual goldfish (Carassius auratus) were observed with variable and constant light sources on opposite sides of a test tank. The DLR was measured with respect to angle (degree) and duration (seconds) of body tilt about the longitudinal axis. After baseline readings were obtained, the intertectal commissure was cut and TL was removed bilaterally. Surgical control fish had only the intertectal commissure cut. Following surgery, TL ablatees showed a significantly reduced DLR compared to controls. The results are consistent with the suggestion by Northmore [1984] that TL may be involved in the processing of luminance information.

Effects of eye position on auditory localization and neural representation of space in superior colliculus of cats.

The maps of visual and auditory space within the superior colliculus are in approximate register both with each other and with the underlying motor maps associated with orienting responses. The fact that eyes and ears can move independently poses a problem for the sensorimotor organization of these two modalities. By monitoring eye and pinna positions in alert, head-fixed cats, we showed that the accuracy of saccadic eye movements to auditory targets was little affected by eye eccentricity (range +/- 15 deg) at the onset of the sound. A possible neural basis for this behavioral compensation was suggested by recordings from superior colliculus neurons. The preferred sound directions of some neurons in the deep layers of this midbrain nucleus exhibited a shift with the direction of gaze, while in others the response throughout the auditory receptive field was either increased or decreased, suggesting that changes in eye position alter the gain of the auditory response.

Recovery of contrast sensitivity during optic nerve regeneration in fish.

Psychophysical experiments on goldfish and sunfish studied the recovery time course of visual contrast detection during optic nerve regeneration. The results showed delayed recovery of detection of positive as compared to negative contrasts, and of high as compared to low spatial frequencies. The findings are related to previous electrophysiological and anatomical results in the fish retinotectal system.

Refractive state, contrast sensitivity, and resolution in the freshwater turtle, Pseudemys scripta elegans, determined by tectal visual-evoked potentials.

Visual-evoked potentials (VEPs) were recorded from the surface of the optic tectum of the freshwater turtle, Pseudemys scripta elegans, in response to phase reversal of square-wave gratings of different spatial frequency and contrast. The refractive state of a group of 12 turtles in air was assessed from VEPs by placing trial lenses in front of the eye. The group mean refraction did not differ significantly from emmetropia, as compared to 4.8 diopters of hyperopia when refracted retinoscopically. The difference was explained by the retinoscopic reflex originating from the interface between vitreous humor and retina. Peak VEP amplitude was approximately linear with log grating contrast; extrapolation to zero VEP amplitude yielded contrast thresholds as low as 1%. High spatial-frequency cutoffs ranged from 4.4-9.9 cycle/deg in different animals, the highest values corresponding to the intercone spacing in the area centralis and to behavioral measures of acuity in a related species.

Ocular dimensions and schematic eyes of freshwater and sea turtles.

Measurements were made of the ocular dimensions from living and frozen eyes of one species of freshwater turtle, Pseudemys scripta elegans, and of three species of marine turtles, Chelonia mydas, Dermochelys cariacea, and Eretmochelys imbricata. Estimates of refractive error by retinoscopy were also obtained with eyes in air and under water. The results suggest that unaccommodated eyes of all four species are approximately emmetropic in air but strongly hyperopic in water. Schematic eyes were calculated for each species in both air and water.

Visual responses of nucleus isthmi in a teleost fish (Lepomis macrochirus).

Extracellular electrical activity was recorded from the nucleus isthmi of the bluegill sunfish (Lepomis macrochirus) in response to brief flashes produced by red light emitting diodes, and other visual stimuli. Metal microelectrodes detected positive spikes outside the nucleus, and negative spikes inside. Spikes of a continuous range of amplitudes up to 1 mV occurred in bursts, spontaneously and visually triggered. The highest amplitude spikes were triggered by the appearance or movement of stimuli throughout the visual field of the contralateral eye. Smaller spikes were triggered by stimuli throughout both visual fields. However, all spiking activity habituated with repeated stimulation in one region of the field. Stimulating at 12 widely spaced positions within the visual field of one eye yielded no consistent differences in the numbers of large spikes evoked. Different penetrations within and around the nucleus also gave uniform distributions of spike numbers. Thus no visuotopic organization was evident. The large spike response evoked by contralateral field stimulation was partially inhibited by a competing stimulus presented to the ipsilateral eye.

Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish--I. Early recovery of dimming sensitivity in tectum and torus longitudinalis.

Refinement and connectivity in the regenerating retinotectal system of goldfish were studied quantitatively by electrophysiological methods. One optic nerve was crushed intraorbitally in fish kept at 25 degrees C. At different postcrush times, visually-evoked multiunit activity was recorded from the superficial layers of tectum, and from the torus longitudinalis. Responses in torus longitudinalis were used as a test of retinotectal connectivity because torus longitudinalis derives a visuotopic map from a tectal projection. The stimulus, effective for both the early retinotectal projection and torus longitudinalis, was a 10 degrees wide vertical black stripe rotated horizontally at 25 degrees/s through both visual fields. Activity from repeated sweeps was averaged to yield receptive field profiles in the horizontal dimension. Normally, profiles from tectum were dual-peaked and 20 degrees wide at half maximum amplitude; torus longitudinalis profiles were bell-shaped and 41 degrees wide. Between 20 and 40 days postcrush, tectum gave broad low-amplitude (25% normal) profiles that were roughly visuotopic. Over the same period, torus longitudinalis gave profiles of relatively high amplitude (69% of normal) that were also broadened but normally visuotopic. The widths of both tectal and torus longitudinalis profiles declined with the same exponential timecourse, reaching normal values by 80-100 days. Torus longitudinalis profiles were on average 21.6 degrees wider than tectal profiles at all stages of regeneration. The results agree with previous anatomical observations showing that optic fibers initially form much enlarged arbors that shrink over time, and suggest that arbors engage in widespread synaptic connections, at least with tecto-torus longitudinalis cells.(ABSTRACT TRUNCATED AT 250 WORDS)

Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish--II. Delayed recovery of sensitivity to small light flashes.

The regenerating retinotectal projection of goldfish was mapped with punctate flashes of light produced by red light-emitting diodes. The characteristics of multiunit receptive fields were studied in fish kept at 25 degrees C at different times after unilateral optic nerve crush. From about 20 days, when the first visually-evoked responses to black-on-white stimuli appeared, until about 40 days, no consistent responses to light-emitting diodes could be obtained, although high-contrast, long-duration light-emitting diode stimuli elicited weak off-responding. At around 40 days, responses to light-emitting diodes reappeared as the amplitude of evoked multiunit activity increased sharply. At their emergence, light-emitting diode-sensitive multiunit receptive fields were irregular and only slightly enlarged, but quickly regained normal shape and size. Conformity to a linear and uniform visuotopography recovered more slowly and, in some individuals, incompletely. The results suggest that "on" and "off" optic fiber systems, probably with small terminal arbors, are functionally expressed at a later time in regeneration than the predominantly "off" system manifested earlier. The different time courses of recovery in these systems explain several aspects of the recovery of visual behavior during optic nerve regeneration.

Behavior evoked by electrical stimulation of the hamster superior colliculus.

Syrian golden hamsters were implanted with fixed or moveable stimulating electrodes aimed at the superior colliculus (SC). Behavior was observed in response to trains of 0.1 ms pulses at 200 Hz while the animals were moving freely in an open arena or in their home cages. At threshold stimulating currents, the responses consisted almost entirely of freezing or contraversive turning, which occurred in two forms: fast turns, resembling orienting movements to sunflower seeds, and slow turns that were smooth and continuous. Other responses, including head raising and lowering, ipsiversive turning and backing movements were seen occasionally. Increasing the stimulating current usually gave a variety of responses, including circling movements, prolonged freezing, ipsilateral movements and running escape behavior. The sites in SC giving freezes at threshold tended to be located superficially (SO and above), or deep (SGP and below), while sites giving turns were in the intermediate layers. Most freeze sites occurred in the rostro-medial SC that represents the upper visual field, while turn sites occurred predominantly in caudo-lateral SC. Apart from the turns, most of the stimulated responses resembled natural defensive behavior, supporting the view that SC in rodents plays a role in organizing responses to predators, as well as in orienting behavior.

Neural activity in the regenerating optic nerve of the goldfish.

1. Retinal ganglion cells of one eye were axotomized in goldfish either by sectioning the contralateral optic tract or by ablating the contralateral lobe of the optic tectum. Between 2 and 40 days later, multiunit activity in response to diffuse light flashes was recorded from the axotomized and normal optic nerves, and from the optic tectum. 2. Two days after tract section, the amplitude of the integrated multiunit response of the axotomized nerve was normal. By 16 days it had fallen to 15% of control values, at which time visual responses carried by the regenerating tract were first recorded in tectum. Activity in the axotomized nerve then recovered gradually. 3. After ablation of one tectal lobe, multiunit responses in the axotomized nerve had not recovered by 40 days. 4. Integrated spontaneous activity in the axotomized nerve was depressed with a similar time course to the depression of light-evoked activity, both after tract section and tectal ablation. 5. Retinal ganglion cell nuclear size, a morphological indicator of the cell body reaction, varied inversely with evoked activity, whether axotomy was by tract section or by tectal ablation. 6. Electrically evoked compound action potentials of normal amplitude could be recorded from an axotomized nerve despite depressed responses to light flashes. 7. It is concluded that optic nerve axotomy in goldfish reduces the number of optic fibres carrying impulses and/or the frequency of their discharge. The effect is closely linked to morphological changes occurring in the retinal ganglion cell bodies. Recovery of impulse activity and morphology depends upon the regenerating optic fibres innervating an appropriate target.

Patterns of deoxyglucose and glucose labeling in the optic tectum of monocularly stimulated bass.

Uniformly labeled deoxyglucose and glucose were used to examine patterns of altered metabolic activity in the optic tectum of largemouth bass. Autoradiographs from fish which viewed moving vertical stripes with one eye show that the metabolites of the two sugars procedure similar patterns of activity-related labeling in the tectum: tangentially arranged bands of increased optical density through the SFGS and the SGC. In addition, aldehyde fixation was found to improve the histological quality of the sections without altering the patterns of labeling.

Recovery of vision in fish after optic nerve crush: a behavioral and electrophysiological study.

Recovery of the visual field was studied during regeneration of the retinotectal projection in bluegill sunfish (Lepomis macrochirus) using a behavioral perimetry technique. Fish were trained to orient ballistically to brief light flashes along the horizontal meridian. After crushing the right optic nerve intraorbitally, orienting to stimuli in the right visual field in different fish reappeared between 32 and 56 days postcrush. On average, recovery of the field center (30 to 150 degrees) occurred in 3 days, the most temporal 30 degrees requiring a further 7 days. Orientation accuracy, measured by the mean absolute error angle, returned to normal 10 to 15 days from the start of recovery. Perimetry was terminated at different times to 152 days postcrush, and the retinotectal projection was mapped electrophysiologically using an automated procedure to characterize multiunit receptive fields (MURFs). At early stages of visual recovery, MURFs associated with strong multiunit discharges were found in the same field regions responsive in behavioral perimetry. The 10- to 15-day recovery of normal orienting accuracy was associated with an increase in the amplitude of multiunit activity, attaining a plateau of 75% of normal. There was also evidence of a long-term decline in MURF area. Early maps showed a roughly normal visutopic order, although abnormalities in MURF size and shape persisted to as much as 152 days postcrush.