Temporal pattern sensitive and nonsensitive responses in the cat's retinal ganglion cells

In order to characterize temporal pattern sensitivity in the cat ganglion cells, a new analysis technique by semi-Markov models which was developed in the previous papers (Tsukada et al., 1975–1977) was applied to input-output relations of the receptive-field. Three types of statistical spot stimuli positioned in the center region of receptive fields were used. Each type of stimulus has an identical histogram in the inter-stimulus intervals and therefore the same mean and variance, but different correlations between adjacent inter-stimulus intervals (Type 1, positive; Type 2, negative; and Type 3, independent processes). From the output spike trains of cat retinal ganglion cells to each stimulus, mean, variance, and histogram were computed. As the result of investigating these data, we could draw the following conclusion from the resultant output interval histograms. The receptive-field-center responses of cat ganglion cells can be classified into two groups (Types L and N) according to the difference of responsiveness to the three types of statistical spot stimuli. A Type L response has the same histogram in interspike intervals for all three stimuli, and is not sensitive to the temporal pattern, while a Type N response has three different forms depending on each type of stimulus showing high sensitivity to the temporal pattern. These results were also simulated by the Markov chain model and discussed with relation to neural coding and classification of ganglion cell types.     

Inhibitory mechanisms within the receptive fields of X-and Y-type retinal ganglion cells of the cat (author's transl)]

Two-stages of the inhibitory mechanisms were assumed within the on-center receptive field (RF) of the cat's retinal ganglion cell on the basis of the following two experiments: 1) Effect of background intensity upon the magnitude of the response to the RF-centered spot of stimulus, and 2) the time course of the inhibitory effect when the additional spot of light is presented in the same RF center region. The first stage is an inhibitory feed-back from horizontal cell to the photoreceptor. Both X-and Y-fields have this feed-back route. By this gain control machanisms, the ganglion cell will respond to the intensity ratio of the spot to the backgound. The second stage of inhibitory mechanism in X-field is the feed-back from sustained amacrine cell to the bipolar cell. Above two stages of feed-back mechanism in X-field explain the strong maintained suppressive effect produced by the additional spot of light. On the other hand, the Y-type ganglion cell will recive the inhibitory input via feed-forward path from trannsient amacrine cell. This explains the transient on- and of f-suppressive effects     

Characteristics of intracellular on - off responses of amacrine cells of the dark-adapted carp retina

The dependence of the amplitude and latent period of intracellular on and off responses of the amacrine cells of the isolated, dark-adapted carp retina on the intensity and diameter of the light spot was investigated. On and off responses of amacrine cells to light were shown to consist of fast depolarization responses with oscillations and spikes superposed upon them. With an increase in the intensity and area of the stimulus the latent period of the on response decreases but that of the off response increases. A near-linear relationship was found between the amplitude of the on response and the logarithm of the diameter of the spot up to 3 mm during changes in stimulus intensity of not more than 4 logarithmic units. With an increase in stimulus intensity the amplitude and zone of summation of the off response are reduced; it is suggested that under these circumstances this decrease may be connected with the different amplitude and temporal characteristics of off processes in the bipolar cells converging on the amacrine cells.     

Spatial properties of goldfish ganglion cells

We systematically classified goldfish ganglion cells according to their spatial summation properties using the same techniques and criteria used in cat and monkey research. Results show that goldfish ganglion cells can be classified as X-, Y-, or W-like based on their responses to contrast-reversal gratings. Like cat X cells, goldfish X-like cells display linear spatial summation. Goldfish Y-like cells, like cat Y cells, respond with frequency doubling at all spatial positions when the contrast-reversal grating consists of high spatial frequencies. There is also a third class of neurons, which is neither X- nor Y-like; many of these cells' properties are similar to those of the "not-X" cells found in the eel retina. Spatial filtering characteristics were obtained for each cell by drifting sinusoidal gratings of various spatial frequencies and contrasts across the receptive field of the cell at a constant temporal rate. The spatial tuning curves of the cell depend on the temporal parameters of the stimulus; at high drift rates, the tuning curves lose their low spatial frequency attenuation. To explore this phenomenon, temporal contrast response functions were derived from the cells' responses to a spatially uniform field whose luminance varied sinusoidally in time. These functions were obtained for the center, the surround, and the entire receptive field. The results suggest that differences in the cells' spatial filtering across stimulus drift rate are due to changes in the interaction of the center and surround mechanisms; at low temporal frequencies, the center and surround responses are out-of-phase and mutually antagonistic, but at higher temporal rates their responses are in-phase and their interaction actually enhances the cell's responsiveness.     

Temporal tuning and nonlinearity of intraretinal pathways in turtle: Effects of temperature,stimulus intensity,and size

Flash responses, amplitude and phase transfer functions, and nonlinearities were measured in turtle retina for pathways with photoreceptor inputs and outputs from horizontal (HC), hyperpolarizing bipolar (HBC), sustained amacrine (AC), and on-off ganglion (GC) cells. Flash responses slowed and attenuated in all cells as temperature decreased. Whitenoise transfer properties of sustained-type cells (HC, HBC, AC) were of low- or bandpass type; highfrequency cut-off (f _c) and phase crossover frequency decreased with temperature. f _c increased as spot diameter was increased. Nonlinearity of these sustained-response pathways (distortion product frequencies in response to a sum-of-sinusoids input probe) increases with intensity and may depend on amplitude saturation limiting. On/off GC synaptic and spike activity increased as spot diameter decreased and intensity increased. Amplitude transfer functions had a low-frequency peak (PSP activity) and monotonically decreasing amplitude vs. frequency shape (spikes and transient PSP activity). Nonlinearity increased with stimulus intensity; it was maximal with 1 mm spot size, less with smaller (500 m) and larger (5 mm) spots. It may depend on the functional equivalent of full-wave rectification (on-off response).This work was supported by NEI grant R01 EY03383     

Goldfish color vision sensitivity is high under light-adapted conditions

The wavelength discrimination threshold of three goldfish was examined in a series of behavioral experiments. Using an auto-shaping technique, detection thresholds were established for 531 and 648 nm spectral increments presented on a 6.6 cd m^–2 white background. Next, discrimination between the wavelengths was established at equal, suprathreshold, intensities. Finally, the intensities of the two stimuli were reduced to establish the intensity threshold for the wavelength discrimination. The results indicate that goldfish, like several mammalian species, can discriminate wavelength at detection threshold intensity. This finding suggests that high color sensitivity is not confined to mammals or dependent upon a very high percentage of wavelength opponent ganglion cells. Rather, high color vision sensitivity may be based upon an inherent sensitivity advantage of wavelength opponent receptive fields compared to non-wavelength opponent receptive fields and be an important selective advantage of wavelength opponency and color vision.     

Transformation of peripheral inputs by the first-order lateral line brainstem nucleus

Extracellular recording techniques were used to record the responses of medial nucleus cells and posterior lateral line nerve fibers in mottled sculpin, Cottus bairdi, and goldfish, Carassius auratus, to a 50-Hz dipole source (vibrating sphere). Responses were characterized in terms of (1) receptive fields that relate responsiveness (spike rate and phase-locking) to the location of the source along the length of the fish, (2) input-output functions that relate responsiveness to vibration amplitude for a fixed source location, and (3) peri-stimulus time histograms that relate responsiveness to time during a sustained period of vibration. Relative to posterior lateral line nerve fibers, medial nucleus cells in both species were similar in showing (1) lower spontaneous and evoked rates of spike activity, (2) greater degrees of adaptation, (3) greater heterogeneity in all response characteristics, and (4) evidence for inhibitory/excitatory interactions. Whereas receptive fields of nerve fibers in both species faithfully reflect both pressure gradient amplitudes (with rate changes) and directions (with phase-angle changes) in the stimulus field, receptive fields of medial nucleus were more difficult to relate to the stimulus field. Some, but not all, receptive fields could be modeled with excitatory center/inhibitory surround and inhibitory center/excitatory surround organizations. Accepted: 26 November 1997     

Selective stabilization of retinotectal synapses by an activity-dependent mechanism

How does each ingrowing retinal fiber select the right spot in the overall retinotopic projection? Chemospecific surface interactions appear to be sufficient only to organize a crude retinotopic map on the tectum during regeneration of the optic nerve of goldfish. Precise retinotopic ordering is achieved via an activity-dependent stabilization of appropriate synapses, based on the correlated activity of neighboring ganglion cells of the same receptive field type in the retina. Four treatments have been found to block the sharpening process: 1) blocking activity of the ganglion cells with intraocular tetrodotoxin (TTX); 2) rearing in total darkness; 3) correlated activation of all ganglion cells via stroboscopic illumination in a featureless environment; 4) block of retinotectal synaptic transmission with alpha-bungarotoxin. These experiments support a role for normal visually driven activity in sharpening the diffuse projection, and demonstrate that the correlated activity of the optic fibers interacts within the postsynaptic cells, probably through the summation of excitatory postsynaptic potentials. Intraocular TTX experiments suggest that a similar mechanism may drive both the formation of ocular dominance patches in fish tectum and kitten visual cortex and the segregation of different receptive field types in the lateral geniculate nucleus. Thus, it may be a general mechanism whereby the diffuse projections of early development are brought to a mature level of organization.     

Habituation and dishabituation mediated by the peripheral and central neural circuits of the siphon of aplysia

The siphon withdrawal response evoked by a weak tactile (water drop) or light stimulus is mediated primarily by neurons in the siphon. Central neurons (abdominal ganglion) contribute very little since the response amplitude and latency are not changed following removal of the abdominal ganglion. Similarly, habituation and dishabituation of this withdrawal response are not different after removal of the abdominal ganglion, indicating that the peripheral neural circuit in the isolated siphon can mediate habituation itself, and thus has many of the properties attributed to central neurons. Responses evoked by electrical stimulation of the siphon nerve habituate, depending upon the stimulus intensity and interval. These habituated responses may be dishabituated by tactile or light stimulation of the siphon. These results show that each neural system, peripheral and central, has an excitatory modulatory influence on the other. Normally adaptive siphon responses must be shaped by the integrated activity of both of these neural systems.     

Simple model for encoding natural images by retinal ganglion cells with nonlinear spatial integration

A central goal in sensory neuroscience is to understand the neuronal signal processing involved in the encoding of natural stimuli. A critical step towards this goal is the development of successful computational encoding models. For ganglion cells in the vertebrate retina, the development of satisfactory models for responses to natural visual scenes is an ongoing challenge. Standard models typically apply linear integration of visual stimuli over space, yet many ganglion cells are known to show nonlinear spatial integration, in particular when stimulated with contrast-reversing gratings. We here study the influence of spatial nonlinearities in the encoding of natural images by ganglion cells, using multielectrode-array recordings from isolated salamander and mouse retinas. We assess how responses to natural images depend on first- and second-order statistics of spatial patterns inside the receptive field. This leads us to a simple extension of current standard ganglion cell models. We show that taking not only the weighted average of light intensity inside the receptive field into account but also its variance over space can partly account for nonlinear integration and substantially improve response predictions of responses to novel images. For salamander ganglion cells, we find that response predictions for cell classes with large receptive fields profit most from including spatial contrast information. Finally, we demonstrate how this model framework can be used to assess the spatial scale of nonlinear integration. Our results underscore that nonlinear spatial stimulus integration translates to stimulation with natural images. Furthermore, the introduced model framework provides a simple, yet powerful extension of standard models and may serve as a benchmark for the development of more detailed models of the nonlinear structure of receptive fields.     

Dynamics of turtle cones

The response dynamics of turtle photoreceptors (cones) were studied by the cross-correlation method using a white-noise-modulated light stimulus. Incremental responses were characterized by the kernels. White-noise-evoked responses with a peak-to-peak excursion of greater than 5 mV were linear, with mean square errors of approximately 8%, a degree of linearity comparable to the horizontal cell responses. Both a spot (0.17 mm diam) and a large field of light produced almost identical kernels. The amplitudes of receptor kernels obtained at various mean irradiances fitted approximately the Weber-Fechner relationship and the mean levels controlled both the amplitude and the response dynamics; kernels were slow and monophasic at low mean irradiance and were fast and biphasic at high mean irradiance. This is a parametric change and is a piecewise linearization. Horizontal cell kernels evoked by the small spot of light were monophasic and slower than the receptor kernels produced by the same stimulus. Larger spots of light or a steady annular illumination transformed the slow horizontal cell kernel into a fast kernel similar to those of the receptors. The slowing down of the kernel waveform was modeled by a simple low-pass circuit and the presumed feedback from horizontal cells onto cones did not appear to play a major role.     

The statistical detection of threshold signals in the retina

1. Photographic records of impulses from single ganglion cells in the cat's retina were made while the retina was stimulated by flashes occurring once a second. Ten flashes at each of several intensities near threshold were used. 2. For the purpose of statistical analysis, the number of impulses (x) falling within a critical period following each flash was used as an index of the response. Histograms of x were plotted and used to calculate rates of transfer of information by the ganglion cell for the case of an ideal experiment, the yes-no choice, in which flashes of intensity I and blanks are to be distinguished. 3. The information rate increased (a) with increasing stimulus intensity and (b) with the number of identical flashes or blanks presented successively in a block. The intensity chosen as threshold by the experimenter, who observed the impulses visually and aurally, corresponded to an average information rate for single flashes of 0.7 bit/flash, compared to the maximum possible rate of 1 bit/flash. A threshold intensity giving 0.4 or more bit/flash, if presented in blocks of six identical flashes, corresponded to 0.95 or more bit/block, or near certainty. Thus the calculation of information rates using the index x provides an estimate of threshold at least as sensitive as those obtained during an experiment, which were made only after observing the responses to five to ten flashes of the same intensity. 4. The index x has statistical properties similar to those of the "index of neural activity" used by Tanner and Swets (1954) in their statistical model of human vision, and represents a possible physical interpretation of their index. However, x gave values (0.5 to 1.5) of the parameter called the slope which were consistently smaller than their values (2.1 to 3.1).     

Sensitivity of a sensory process to short time delays: A study in pattern induced flicker colors (PIFCs)

Pattern induced flicker colors (PIFCs) were generated by means of a modified version of Benham's top, the stimulus pattern of which could be varied continuously during stimulation by the human subjects. The sensitivity of the color sensation to small phase shifts between the periodic stimuli on neighboring retinal areas was recorded under several conditions of stimulus parameters. A mathematical model was developed to describe the influence of the stimulus parameters on the recorded sensory effect. Concerning the underlying neurophysiological processes, a hypothesis is advanced according to which the phase sensitive lateral interaction within the retina changes the spatial excitation distribution within color coding receptive fields of the retinal ganglion cells. The resulting ganglion cell excitation is supposed to generate PIFCs.     

Receptive field types in the lateral geniculate body and their frequency characteristics]

Time amplitude -- frequency characteristics of the I and II types of receptive fields (RF) of lateral geniculate and their dependence on the contrast and spatial parameters of the light stimulus were studied. It is shown that the frequency characteristics of the RF I type depends on the contrast and area of the light stimulus, the higher being the contrast at a small area the smaller are the low frequencies. However at a large area of the stimulus the inhibition of low frequencies is greater at a small contrast. The transmitting band of frequency characteristics of RF II type does not depend on the contrast at a small area of the stimulus, at a large area a fall of low frequencies takes place at high contrasts of the stimulus. Such different behaviour of the receptive fields is explained by the models, which take into account RF spatial characteristics.     

Configurational pattern discrimination responsible for dishabituation in common toads Bufo bufo (L.): Behavioral tests of the predictions of a neural model

Summary Recently, a neural model of visual pattern discrimination for stimulus-specific habituation was developed, based on previous behavioral studies which demonstrated that toads exhibit a dishabituation hierarchy for different worm-like stimuli. The model suggests that visual objects are represented by temporal coding and predicts that the dishabituation hierarchy changes when the stimulus/background contrast direction is reversed or the stimulus size is varied. The behavioral experiments reported in this paper were designed to test these predictions, (1) For a pair of stimuli from the contrast reversal prediction, the experimental results validated the theory. (2) For a pair of stimuli from the size reduction prediction, the experimental results failed to validate the theory. Further experiments concerning size effects suggest that configurai visual pattern discrimination in toads exhibits size invariance. (3) Inspired by the Groves-Thompson account of habituation, we found that dishabituation by a second stimulus has a separate process from habituation to a first stimulus. This paper serves as an example of a fruitful dialogue between experimentation and modeling, crucial for understanding brain functions.Abbreviations a-h worm-like stimulus patterns - AT anterior thalamus - ERF excitatory receptive field - IRF inhibitory receptive field - RF receptive field - R2 to R4 retinal ganglion cell types - vMP posterior ventromedial pallium     

Discriminative Learning of Receptive Fields from Responses to Non-Gaussian Stimulus Ensembles

Analysis of sensory neurons'' processing characteristics requires simultaneous measurement of presented stimuli and concurrent spike responses. The functional transformation from high-dimensional stimulus space to the binary space of spike and non-spike responses is commonly described with linear-nonlinear models, whose linear filter component describes the neuron''s receptive field. From a machine learning perspective, this corresponds to the binary classification problem of discriminating spike-eliciting from non-spike-eliciting stimulus examples. The classification-based receptive field (CbRF) estimation method proposed here adapts a linear large-margin classifier to optimally predict experimental stimulus-response data and subsequently interprets learned classifier weights as the neuron''s receptive field filter. Computational learning theory provides a theoretical framework for learning from data and guarantees optimality in the sense that the risk of erroneously assigning a spike-eliciting stimulus example to the non-spike class (and vice versa) is minimized. Efficacy of the CbRF method is validated with simulations and for auditory spectro-temporal receptive field (STRF) estimation from experimental recordings in the auditory midbrain of Mongolian gerbils. Acoustic stimulation is performed with frequency-modulated tone complexes that mimic properties of natural stimuli, specifically non-Gaussian amplitude distribution and higher-order correlations. Results demonstrate that the proposed approach successfully identifies correct underlying STRFs, even in cases where second-order methods based on the spike-triggered average (STA) do not. Applied to small data samples, the method is shown to converge on smaller amounts of experimental recordings and with lower estimation variance than the generalized linear model and recent information theoretic methods. Thus, CbRF estimation may prove useful for investigation of neuronal processes in response to natural stimuli and in settings where rapid adaptation is induced by experimental design.     

Temporal pattern discrimination within the receptive field of cat retinal ganglion cells

ON-center and OFF-center receptive fields of cat retinal ganglion cells can be divided into two categories: sensitive (type N) and insensitive (type L) to three statistical temporal visual stimuli with different second order statistics but identical first order statistics (Tsukada et al. 1982). The temporal pattern sensitivity of type N response is closely related to the nonlinear stage of Y cells depending on the interaction between center and surround mechanism. The temporal pattern sensitivity of type N responses has a spatial profile within the receptive field; it is highly sensitive in the center region of the receptive field and less sensitive toward the field periphery. The temporal pattern sensitivity in the center region of the receptive field to statistical properties (irregular or regular) of a surrounding flash annulus shows modulation like a switching element: when the surrounding area is stimulated by a more regular flash stimulus with normal distribution of inter-stimulus intervals the system is sensitive (switching on) to the temporal pattern, while a change to an irregular one with an exponential distribution makes it insensitive (switching off) to the temporal pattern.     

Nonlinear characteristics in the Frog's visual system

The receptive fields of retinal fibers in the visual tectum of the frog are mapped with different techniques and the spatial summation characteristics are examined, by presenting stimuli of various shapes and sizes in the center of the receptive field. When the size is increased gradually from the center of the stimulus, for constant stimulus intensity, the maximum response is obtained for stimuli of approximately the size of the most responsive part of the RF. Using a clustering technique to obtain stimuli that are part of the RF and combinations of these parts, it is evident that the spatial summation characteristics are not linear. A model is developed that describes the nonlinear form of these results, based on a power law.     

Responses of nervous elements of the visual cortex of the chipmunk Eutamias sibiricus to moving and stationary stimuli]

The receptive field organization of cortical units has been studied in experiments with testing by moving and stationary light spots. The size of the receptive fields varied from 3 degrees to 10 degrees. Receptive fields which were tested by a stationary light spot exhibited various types of organization. Some of the neurons produced extensive excitatory on- and off-responses to stimulation by a light spot. Neuronal excitation evoked by light decreased if the stimulus was near the field boundary. Some of the neurons produced either on- or off-responses in any point of the receptive field. A small part of neurons had receptive fields with on- and off-reactions in the center, and either on- or off-responses at the peripheral zones. Most of the neurons exhibited specialization with respect to high-speed motion.     

Delayed responses of ganglion cells in the frog retina: the influence of stimulus parameters upon the discharge pattern

The delayed response from frog retinal ganglion cells is preceded by a long silent period which has been shown to depend upon (i) intensity of the stimulus light flash, (ii) background illumination, and (iii) instantaneous level of adaptation. Also the duration of the delayed response and the total number of spikes elicited are functions of these three parameters. A linear relationship has been found between the silent period and both delayed response duration and total number of spikes. Double-flash experiments indicate that the ganglion cell output is strongly inhibited during the silent period. Experiments using an inhomogenous stimulus field have led to the conclusion that parts of the receptive field contribute independently to the delayed response.Supported by the Deutsche Forschungsgemeinschaft.S. G. P. was a postdoctoral fellow supported by a U. S. Public Health Service grant, NIH 1 F 2 NB 24,455-01.