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J H van Hateren

Publications and source records attributed to J H van Hateren.

At least 19 recordsLinked to original sources

Encoding of naturalistic optic flow by a population of blowfly motion-sensitive neurons.

In sensory systems information is encoded by the activity of populations of neurons. To analyze the coding properties of neuronal populations sensory stimuli have usually been used that were much simpler than those encountered in real life. It has been possible only recently to stimulate visual interneurons of the blowfly with naturalistic visual stimuli reconstructed from eye movements measured during free flight. Therefore we now investigate with naturalistic optic flow the coding properties of a small neuronal population of identified visual interneurons in the blowfly, the so-called VS and HS neurons. These neurons are motion sensitive and directionally selective and are assumed to extract information about the animal's self-motion from optic flow. We could show that neuronal responses of VS and HS neurons are mainly shaped by the characteristic dynamical properties of the fly's saccadic flight and gaze strategy. Individual neurons encode information about both the rotational and the translational components of the animal's self-motion. Thus the information carried by individual neurons is ambiguous. The ambiguities can be reduced by considering neuronal population activity. The joint responses of different subpopulations of VS and HS neurons can provide unambiguous information about the three rotational and the three translational components of the animal's self-motion and also, indirectly, about the three-dimensional layout of the environment.

Animals↗

The photocurrent response of human cones is fast and monophasic.

BACKGROUND: The precise form of the light response of human cone photoreceptors in vivo has not been established with certainty. To investigate the response shape we compare the predictions of a recent model of transduction in primate cone photoreceptors with measurements extracted from human cones using the paired-flash electroretinogram method. As a check, we also compare the predictions with previous single-cell measurements of ground squirrel cone responses. RESULTS: The predictions of the model provide a good description of the measurements, using values of parameters within the range previously determined for primate retina. The dim-flash response peaks in about 20 ms, and flash responses at all intensities are essentially monophasic. Three time constants in the model are extremely short: the two time constants for inactivation (of visual pigment and of transducin/phosphodiesterase) are around 3 and 10 ms, and the time constant for calcium equilibration lies in the same range. CONCLUSION: The close correspondence between experiment and theory, using parameters previously derived for recordings from macaque retina, supports the notion that the electroretinogram approach and the modelling approach both provide an accurate estimate of the cone photoresponse in the living human eye. For reasons that remain unclear, the responses of isolated photoreceptors from the macaque retina, recorded previously using the suction pipette method, are considerably slower than found here, and display biphasic kinetics.

Animals↗

Representation of behaviourally relevant information by blowfly motion-sensitive visual interneurons requires precise compensatory head movements.

Flying blowflies shift their gaze by saccadic turns of body and head, keeping their gaze basically fixed between saccades. For the head, this results in almost pure translational optic flow between saccades, enabling visual interneurons in the fly motion pathway to extract information about translation of the animal and thereby about the spatial layout of the environment. There are noticeable differences between head and body movements during flight. Head saccades are faster and shorter than body saccades, and the head orientation is more stable between saccades than the body orientation. Here, we analyse the functional importance of these differences by probing visual interneurons of the blowfly motion pathway with optic flow based on either head movements or body movements, as recorded accurately with a magnetic search coil technique. We find that the precise head-body coordination is essential for the visual system to separate the translational from the rotational optic flow. If the head were tightly coupled to the body, the resulting optic flow would not contain the behaviourally important information on translation. Since it is difficult to resolve head orientation in many experimental paradigms, even when employing state-of-the-art digital video techniques, we introduce a 'headifying algorithm', which transforms the time-dependent body orientation in free flight into an estimate of head orientation. We show that application of this algorithm leads to an estimated head orientation between saccades that is sufficiently stable to enable recovering information on translation. The algorithm may therefore be of practical use when head orientation is needed but cannot be measured.

Algorithms↗

Phototransduction in primate cones and blowfly photoreceptors: different mechanisms, different algorithms, similar response.

Phototransduction in primate cones is compared with phototransduction in blowfly photoreceptor cells. Phototransduction in the two cell types utilizes not only different molecular mechanisms, but also different signal processing steps, producing range compression, contrast constancy, and an intensity-dependent integration time. The dominant processing step in the primate cone is a strongly compressive nonlinearity due to cGMP hydrolysis by phosphodiesterase. In the blowfly photoreceptor a considerable part of the range compression is performed by the nonlinear membrane of the cell. Despite these differences, both photoreceptor cell types are similarly effective in compressing the wide range of naturally occurring intensities, and in converting intensity variations into contrast variations. A direct comparison of the responses to a natural time series of intensities, simulated in the cone and measured in the blowfly photoreceptor, shows that the responses are quite similar.

Adaptation, Ocular↗

On the computations analyzing natural optic flow: quantitative model analysis of the blowfly motion vision pathway.

For many animals, including humans, the optic flow generated on the eyes during locomotion is an important source of information about self-motion and the structure of the environment. The blowfly has been used frequently as a model system for experimental analysis of optic flow processing at the microcircuit level. Here, we describe a model of the computational mechanisms implemented by these circuits in the blowfly motion vision pathway. Although this model was originally proposed based on simple experimenter-designed stimuli, we show that it is also capable to quantitatively predict the responses to the complex dynamic stimuli a blowfly encounters in free flight. In particular, the model visual system exploits the active saccadic gaze and flight strategy of blowflies in a similar way, as does its neuronal counterpart. The model circuit extracts information about translation velocity in the intersaccadic intervals and thus, indirectly, about the three-dimensional layout of the environment. By stepwise dissection of the model circuit, we determine which of its components are essential for these remarkable features. When accounting for the responses to complex natural stimuli, the model is much more robust against parameter changes than when explaining the neuronal responses to simple experimenter-defined stimuli. In contrast to conclusions drawn from experiments with simple stimuli, optimization of the parameter set for different segments of natural optic flow stimuli do not indicate pronounced adaptational changes of these parameters during long-lasting stimulation.

Adaptation, Physiological↗

Motion adaptation leads to parsimonious encoding of natural optic flow by blowfly motion vision system.

Neurons sensitive to visual motion change their response properties during prolonged motion stimulation. These changes have been interpreted as adaptive and were concluded, for instance, to adjust the sensitivity of the visual motion pathway to velocity changes or to increase the reliability of encoding of motion information. These conclusions are based on experiments with experimenter-designed motion stimuli that differ substantially with respect to their dynamical properties from the optic flow an animal experiences during normal behavior. We analyze for the first time motion adaptation under natural stimulus conditions. The experiments are done on the H1-cell, an identified neuron in the blowfly visual motion pathway that has served in many previous studies as a model system for visual motion computation. We reconstructed optic flow perceived by a blowfly in free flight and used this behaviorally generated optic flow to study motion adaptation. A variety of measures (variability in spike count, response latency, jitter of spike timing) suggests that the coding quality does not improve with prolonged stimulation. However, although the number of spikes decreases considerably during stimulation with natural optic flow, the amount of information that is conveyed stays nearly constant. Thus the information per spike increases, and motion adaptation leads to parsimonious coding without sacrificing the reliability with which behaviorally relevant information is encoded.

Action Potentials↗

Function of a fly motion-sensitive neuron matches eye movements during free flight.

Sensing is often implicitly assumed to be the passive acquisition of information. However, part of the sensory information is generated actively when animals move. For instance, humans shift their gaze actively in a sequence of saccades towards interesting locations in a scene. Likewise, many insects shift their gaze by saccadic turns of body and head, keeping their gaze fixed between saccades. Here we employ a novel panoramic virtual reality stimulator and show that motion computation in a blowfly visual interneuron is tuned to make efficient use of the characteristic dynamics of retinal image flow. The neuron is able to extract information about the spatial layout of the environment by utilizing intervals of stable vision resulting from the saccadic viewing strategy. The extraction is possible because the retinal image flow evoked by translation, containing information about object distances, is confined to low frequencies. This flow component can be derived from the total optic flow between saccades because the residual intersaccadic head rotations are small and encoded at higher frequencies. Information about the spatial layout of the environment can thus be extracted by the neuron in a computationally parsimonious way. These results on neuronal function based on naturalistic, behaviourally generated optic flow are in stark contrast to conclusions based on conventional visual stimuli that the neuron primarily represents a detector for yaw rotations of the animal.

Animals↗

Function and coding in the blowfly H1 neuron during naturalistic optic flow.

Naturalistic stimuli, reconstructed from measured eye movements of flying blowflies, were replayed on a panoramic stimulus device. The directional movement-sensitive H1 neuron was recorded from blowflies watching these stimuli. The response of the H1 neuron is dominated by the response to fast saccadic turns into one direction. The response between saccades is mostly inhibited by the front-to-back optic flow caused by the forward translation during flight. To unravel the functional significance of the H1 neuron, we replayed, in addition to the original behaviorally generated stimulus, two targeted stimulus modifications: (1) a stimulus in which flow resulting from translation was removed (this stimulus produced strong intersaccadic responses); and (2) a stimulus in which the saccades were removed by assuming that the head follows the smooth flight trajectory (this stimulus produced alternating zero or nearly saturating spike rates). The responses to the two modified stimuli are strongly different from the response to the original stimulus, showing the importance of translation and saccades for the H1 response to natural optic flow. The response to the original stimulus thus suggests a double function for the H1 neuron, assisting two major classes of movement-sensitive output neurons targeted by H1. First, its strong response to saccades may function as a saccadic suppressor (via one of its target neurons) for cells involved in figure-ground discrimination. Second, its intersaccadic response may increase the signal-to-noise ratio (SNR) of wide-field neurons involved in detecting translational optic flow between saccades, in particular when flying speeds are low or when object distances are large.

Action Potentials↗

Saccadic head and thorax movements in freely walking blowflies.

Visual information processing is adapted to the statistics of natural visual stimuli, and these statistics depend to a large extent on the movements of an animal itself. To investigate such movements in freely walking blowflies, we measured the orientation and position of their head and thorax, with high spatial and temporal accuracy. Experiments were performed on Calliphora vicina, Lucilia cuprina and L. caesar. We found that thorax and head orientation of walking flies is typically different from the direction of walking, with differences of 45 degrees common. During walking, the head and the thorax turn abruptly, with a frequency of 5-10 Hz and angular velocities in the order of 1,000 degrees /s. These saccades are stereotyped: head and thorax start simultaneously, with the head turning faster, and finishing its turn before the thorax. The changes in position during walking are saccade-like as well, occurring synchronously, but on average slightly after the orientation saccades. Between orientation saccades the angular velocities are low and the head is held more stable than the thorax. We argue that the strategy of turning by saccades improves the performance of the visual system of blowflies.

Animals↗

Asymmetric dynamics of adaptation after onset and offset of flicker.

We measured human psychophysical detection thresholds for test pulses which are superimposed on spatially homogeneous backgrounds that have abrupt onsets and offsets of high-contrast 25 Hz flicker. After the onset of the background flicker, test thresholds reach their steady-state levels within 20-60 ms. After the offset of the background flicker, test thresholds remain elevated above their steady-state level for much longer durations. Adaptation after onsets and offsets of background flicker is modeled with a divisive gain control that is activated by temporal contrast. We show that a feedback structure for the gain control can explain the asymmetric dynamics observed after onsets and offsets of the background contrast. Finally, we measure detection thresholds for tests presented on steadily flickering backgrounds as a function of the contrast of the background flicker. We show that the divisive feedback model for contrast gain control can describe these results as well.

Adaptation, Ocular↗

FliMax, a novel stimulus device for panoramic and highspeed presentation of behaviourally generated optic flow.

A high-speed panoramic visual stimulation device is introduced which is suitable to analyse visual interneurons during stimulation with rapid image displacements as experienced by fast moving animals. The responses of an identified motion sensitive neuron in the visual system of the blowfly to behaviourally generated image sequences are very complex and hard to predict from the established input circuitry of the neuron. This finding suggests that the computational significance of visual interneurons can only be assessed if they are characterised not only by conventional stimuli as are often used for systems analysis, but also by behaviourally relevant input.

Animals↗

Recovery from contrast adaptation matches ideal-observer predictions.

Recovery from contrast adaptation was studied in psychophysical experiments. We measured detection thresholds for a test pulse presented on a photopic background as a function of the time after the offset of a high-contrast flicker of the background. The decrease of thresholds with time is well described by a power-law function. Thresholds for tests presented at 640 ms after the offset of the background contrast are still significantly elevated above the threshold measured when the observers have completely adapted to a steady background. We compare the psychophysical data with contrast estimates of ideal-observer models. A match between the results for human and ideal observers can be obtained when the ideal observer is limited by noise. For a quantitative match, we assume that the ideal observer performs a Bayesian calculation on its noise-perturbed input, sampled every 10-20 ms. For the Bayesian calculation we assume a prior probability distribution function for the input contrast that has a lower cutoff at the standard deviation of the noise.

Adaptation, Physiological↗

Processing of natural temporal stimuli by macaque retinal ganglion cells.

This study quantifies the performance of primate retinal ganglion cells in response to natural stimuli. Stimuli were confined to the temporal and chromatic domains and were derived from two contrasting environments, one typically northern European and the other a flower show. The performance of the cells was evaluated by investigating variability of cell responses to repeated stimulus presentations and by comparing measured to model responses. Both analyses yielded a quantity called the coherence rate (in bits per second), which is related to the information rate. Magnocellular (MC) cells yielded coherence rates of up to 100 bits/sec, rates of parvocellular (PC) cells were much lower, and short wavelength (S)-cone-driven ganglion cells yielded intermediate rates. The modeling approach showed that for MC cells, coherence rates were generated almost exclusively by the luminance content of the stimulus. Coherence rates of PC cells were also dominated by achromatic content. This is a consequence of the stimulus structure; luminance varied much more in the natural environment than chromaticity. Only approximately one-sixth of the coherence rate of the PC cells derived from chromatic content, and it was dominated by frequencies below 10 Hz. S-cone-driven ganglion cells also yielded coherence rates dominated by low frequencies. Below 2-3 Hz, PC cell signals contained more power than those of MC cells. Response variation between individual ganglion cells of a particular class was analyzed by constructing generic cells, the properties of which may be relevant for performance higher in the visual system. The approach used here helps define retinal modules useful for studies of higher visual processing of natural stimuli.

Action Potentials↗

Information theoretical evaluation of parametric models of gain control in blowfly photoreceptor cells.

Models are developed and evaluated that are able to describe the response of blowfly photoreceptor cells to natural time series of intensities. Evaluation of the models is performed using an information theoretical technique that evaluates the performance of the models in terms of a coherence function and a derived coherence rate (in bit/s). Performance is gauged against a maximum expected coherence rate determined from the repeatability of the response to the same stimulus. The best model performs close to this maximum performance, and consists of a cascade of two divisive feedback loops followed by a static nonlinearity. The first feedback loop is fast, effectively compressing fast and large transients in the stimulus. The second feedback loop also contains slow components, and is responsible for slow adaptation in the photoreceptor in response to large steps in intensity. Any remaining peaks that would drive the photoreceptor out of its dynamic range are handled by the final compressive nonlinearity.

Adaptation, Ocular↗

Independent component analysis of natural image sequences yields spatio-temporal filters similar to simple cells in primary visual cortex.

Simple cells in the primary visual cortex process incoming visual information with receptive fields localized in space and time, bandpass in spatial and temporal frequency, tuned in orientation, and commonly selective for the direction of movement. It is shown that performing independent component analysis (ICA) on video sequences of natural scenes produces results with qualitatively similar spatio-temporal properties. Whereas the independent components of video resemble moving edges or bars, the independent component filters, i.e. the analogues of receptive fields, resemble moving sinusoids windowed by steady Gaussian envelopes. Contrary to earlier ICA results on static images, which gave only filters at the finest possible spatial scale, the spatio-temporal analysis yields filters at a range of spatial and temporal scales. Filters centred at low spatial frequencies are generally tuned to faster movement than those at high spatial frequencies.

Models, Biological↗

Using miniature sensor coils for simultaneous measurement of orientation and position of small, fast-moving animals.

A system is described that measures, with a sampling frequency of 1 kHz, the orientation and position of a blowfly (Calliphora vicina) flying in a volume of 0.4 x 0.4 x 0.4 m3. Orientation is measured with a typical accuracy of 0.5 degrees, and position with a typical accuracy of 1 mm. This is accomplished by producing a time-varying magnetic field with three orthogonal pairs of field coils, driven sinusoidally at frequencies of 50, 68, and 86 kHz, respectively. Each pair induces a voltage at the corresponding frequency in each of three miniature orthogonal sensor coils mounted on the animal. The sensor coils are connected via thin (12-microm) wires to a set of nine lock-in amplifiers, each locking to one of the three field frequencies. Two of the pairs of field coils produce approximately homogeneous magnetic fields, which are necessary for reconstructing the orientation of the animal. The third pair produces a gradient field, which is necessary for reconstructing the position of the animal. Both sensor coils and leads are light enough (0.8-1.6 mg for three sensor coils of 40-80 windings, and 6.7 mg/m for the leads, causing a maximal load of approximately 5.7 mg) not to hinder normal flight of the animal (typical weight 80 mg). In general, the system can be used for high-speed recordings of head, eye or limb movements, where a wire connection is possible, but the mechanical load on the moving parts needs to be very small.

Animals↗

Independent component filters of natural images compared with simple cells in primary visual cortex.

Properties of the receptive fields of simple cells in macaque cortex were compared with properties of independent component filters generated by independent component analysis (ICA) on a large set of natural images. Histograms of spatial frequency bandwidth, orientation tuning bandwidth, aspect ratio and length of the receptive fields match well. This indicates that simple cells are well tuned to the expected statistics of natural stimuli. There is no match, however, in calculated and measured distributions for the peak of the spatial frequency response: the filters produced by ICA do not vary their spatial scale as much as simple cells do, but are fixed to scales close to the finest ones allowed by the sampling lattice. Possible ways to resolve this discrepancy are discussed.

Animals↗