Rapid Dynamics of Contrast Responses in the Cat Primary Visual Cortex

The visual information we receive during natural vision changes rapidly and continuously. The visual system must adapt to the spatiotemporal contents of the environment in order to efficiently process the dynamic signals. However, neuronal responses to luminance contrast are usually measured using drifting or stationary gratings presented for a prolonged duration. Since motion in our visual field is continuous, the signals received by the visual system contain an abundance of transient components in the contrast domain. Here using a modified reverse correlation method, we studied the properties of responses of neurons in the cat primary visual cortex to different contrasts of grating stimuli presented statically and transiently for 40 ms, and showed that neurons can effectively discriminate the rapidly changing contrasts. The change in the contrast response function (CRF) over time mainly consisted of an increment in contrast gain (CRF shifts to left) in the developing phase of temporal responses and a decrement in response gain (CRF shifts downward) in the decay phase. When the distribution range of stimulus contrasts was increased, neurons demonstrated decrement in contrast gain and response gain. Our results suggest that contrast gain control (contrast adaptation) and response gain control mechanisms are well established during the first tens of milliseconds after stimulus onset and may cooperatively mediate the rapid dynamic responses of visual cortical neurons to the continuously changing contrast. This fast contrast adaptation may play a role in detecting contrast contours in the context of visual scenes that are varying rapidly.

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title: Independence of luminance and contrast in natural scenes and in the early visual system
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title: Contrast gain control in the cat's visual system.
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title: Contrast adaptation in striate cortex of macaque
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title: Cellular Mechanisms of Long-Lasting Adaptation in Visual Cortical Neurons In Vitro
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title: Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function.
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title: Temporal coding of contrast in primary visual cortex: when, what, and why.
abstract: How do neurons in the primary visual cortex (V1) encode the contrast of a visual stimulus? In this paper, the information that V1 responses convey about the contrast of static visual stimuli is explicitly calculated. These responses often contain several easily distinguished temporal components, which will be called latency, transient, tonic, and off. Calculating the information about contrast conveyed in each component and in groups of components makes it possible to delineate aspects of the temporal structure that may be relevant for contrast encoding. The results indicate that as much or more contrast-related information is encoded into the temporal structure of spike train responses as into the firing rate and that the temporally coded information is manifested most strongly in the latency to response onset. Transient, tonic, and off responses contribute relatively little. The results also reveal that temporal coding is important for distinguishing subtle contrast differences, whereas firing rates are useful for gross discrimination. This suggests that the temporal structure of neurons' responses may extend the dynamic range for contrast encoding in the primate visual system.

title: Temporal dynamics of contrast gain in single cells of the cat striate cortex.
abstract: The response amplitude of cat striate cortical cells is usually reduced after exposure to high-contrast stimuli. The temporal characteristics and contrast sensitivity of this phenomenon were explored by stimulating cortical cells with drifting gratings in which contrast sequentially incremented and decremented in stepwise fashion over time. All responses showed a clear hysteresis, in which contrast gain dropped on average 0.36 log unit and then returned to baseline values within 60 s. Noticeable gain adjustments were seen in as little as 3 s and with peak contrasts as low as 3%. Contrast adaptation was absent in responses from LGN cells. Adaptation was found to depend on temporal frequency of stimulation, with greater and more rapid adaptation at higher temporal frequencies. Two different tests showed that the mechanism controlling response reduction was influenced primarily by stimulus contrast rather than response amplitude. These results support the existence of a rapid and sensitive cortically based system that normalizes the output of cortical cells as a function of local mean contrast. Control of the adaptation appears to arise at least in part across a population of cells, which is consistent with the idea that the gain control serves to limit the information converging from many cells onto subsequent processing areas.

title: Dynamic contrast change produces rapid gain control in visual cortex
abstract: During normal vision, objects moving in the environment, our own body movements and our eye movements ensure that the receptive fields of visual neurons are being presented with continually changing contrasts. Thus, the visual input during normal behaviour differs from the type of stimuli traditionally used to study contrast coding, which are presented in a step‐like manner with abrupt changes in contrast followed by prolonged exposure to a constant stimulus. The abrupt changes in contrast typically elicit brief periods of intense firing with low variability called onset transients. Onset transients provide the visual system with a powerful and reliable cue that the visual input has changed. In this paper we investigate visual processing in the primary visual cortex of cats in response to stimuli that change contrast dynamically. We show that 1–4 s presentations of dynamic increases and decreases in contrast can generate stronger contrast gain control than several minutes exposure to a stimulus of constant contrast. Thus, transient mechanisms of contrast coding are not only less variable than sustained responses but are also more rapid and flexible. Finally, we propose a quantitative model of contrast coding which accounts for changes in spike rate over time in response to dynamically changing image contrast.

title: Natural scene statistics at the centre of gaze.
abstract: Early stages of visual processing may exploit the characteristic structure of natural visual stimuli. This structure may differ from the intrinsic structure of natural scenes, because sampling of the environment is an active process. For example, humans move their eyes several times a second when looking at a scene. The portions of a scene that fall on the fovea are sampled at high spatial resolution, and receive a disproportionate fraction of cortical processing. We recorded the eye positions of human subjects while they viewed images of natural scenes. We report that active selection affected the statistics of the stimuli encountered by the fovea, and also by the parafovea up to eccentricities of 4 degrees. We found two related effects. First, subjects looked at image regions that had high spatial contrast. Second, in these regions, the intensities of nearby image points (pixels) were less correlated with each other than in images selected at random. These effects could serve to increase the information available to the visual system for further processing. We show that both of these effects can be simply obtained by constructing an artificial ensemble comprised of the highest-contrast regions of images.

title: Striate cortex of monkey and cat: contrast response function.
abstract: 1. We measured the responses of 247 neurons recorded from the striate cortex of monkeys and cats as a function of the contrast intensity of luminance-modulated spatialtemporal sine-wave grating patterns to provide a qualitative description and a quantitative mathematical formulation of the contast response function (CRF). 2. Qualitatively, it is possible to provide a general description of the contrast response function for the majority of cells as follows: as the luminance contrast of a pattern increases, the response increases in a relatively linear fashion over approximately 50-607o of the response range (generally less than I log unit along the contrast range), the slope of the function then begins a rapid compression to an asymptotic maximum-saturation response level. There is, however, a great deal of variation. from cell to cell, in the exact shape and location of the CRF. 3. Quantitatively, the responses of each cell were analyzed in terms of the leastsquares (parameter optimized) best fit using four different mathematical functions: linear, logarithmic power, and hyperbolic ratio. The results of this procedure showed that, across the range of contrasts measured ( 1.4567o), the hypcrbolic ratio (H ratio) provided the best fit for the vast majority of striate cells: some 7O9o f the cells were best fitted by the H ratio and further, averaged across all cells, the H ratio produced the least average residual variance. 4. The contrast response function is an important factor when considering the spatial properties of cortical cells; nonlinearities in the CRF (compression and saturation) will necessarily influence the spatial tuning. We therefore measured the CRF at different spatial frequencies and used the parameters of the H ratio to test the predictions of two general classes of models. If the overall gain, compression, and saturation are set by the absolute response level (response-set gain), then the CRFs measured at different frequencies should shift horizontally along the contrast axis. Results show that the measured CRFs (tested on the same cell using different spatial frequencies) were shifted primarily vertically, suggesting that the gain, compression, and saturation were set by the absolute contrast level (contrast-set gain), relatively independent of spatial frequency; in terms of the H ratio, the semisaturation contrast and the exponent were relatively constant in comparison to the asymptotic saturation response. Thus, the spatial frequency response functions are relatively constant when measured at different stimulus contrasts. 5. There is a great deal of variation in the location of the dynamic response range, from cell to cell, along the contrast axis: some cells distribute their dynamic response range over the first lOVo of contrast, others the second, etc. (relatively independent of preferred spatial frequency). One might expect this range variation to be an important factor in behavioral contrast discrimination. To provide an indication of the average population response as a function of contrast, all cells were averaged together (percent response relative to each cell 's maximum): the slope of the bcst-fitt ing [nwer function (0.77) falls well within the range of estimates found for human psychophysical contrast discrimination functions.

title: Information Conveyed by Onset Transients in Responses of Striate Cortical Neurons
abstract: Normal eye movements ensure that the visual world is seen episodically, as a series of often stationary images. In this paper we characterize the responses of neurons in striate cortex to stationary grating patterns presented with abrupt onset. These responses are distinctive. In most neurons the onset of a grating gives rise to a transient discharge that decays with a time constant of 100 msec or less. The early stages of response have higher contrast gain and higher response gain than later stages. Moreover, the variability of discharge during the onset transient is disproportionately low. These factors together make the onset transient an information-rich component of response, such that the detectability and discriminability of stationary gratings grows rapidly to an early peak, within 150 msec of the onset of the response in most neurons. The orientation selectivity of neurons estimated from the first 150 msec of discharge to a stationary grating is indistinguishable from the orientation selectivity estimated from longer segments of discharge to moving gratings. Moving gratings are ultimately more detectable than stationary ones, because responses to the former are continuously renewed. The principal characteristics of the response of a neuron to a stationary grating—the initial high discharge rate, which decays rapidly, and the change of contrast gain with time—are well captured by a model in which each excitatory synaptic event leads to an immediate reduction in synaptic gain, from which recovery is slow.

title: Gain control from beyond the classical receptive field in primate primary visual cortex
abstract: Gain control is a salient feature of information processing throughout the visual system. Heeger (1991, 1992) described a mechanism that could underpin gain control in primary visual cortex (V1). According to this model, a neuron's response is normalized by dividing its output by the sum of a population of neurons, which are selective for orientations covering a broad range. Gain control in this scheme is manifested as a change in the semisaturation constant (contrast gain) of a V1 neuron. Here we examine how flanking and annular gratings of the same or orthogonal orientation to that preferred by a neuron presented beyond the receptive field modulate gain in V1 neurons in anesthetized marmosets (Callithrix jacchus). To characterize how gain was modulated by surround stimuli, the Michaelis–Menten equation was fitted to response versus contrast functions obtained under each stimulus condition. The modulation of gain by surround stimuli was modelled best as a divisive reduction in response gain. Response gain varied with the orientation of surround stimuli, but was reduced most when the orientation of a large annular grating beyond the classical receptive field matched the preferred orientation of neurons. The strength of surround suppression did not vary significantly with retinal eccentricity or laminar distribution. In the marmoset, as in macaques (Angelucci et al., 2002a, b), gain control over the sort of distances reported here (up to 10 deg) may be mediated by feedback from extrastriate areas.

title: Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development.
abstract: 1. Most studies of cortical neurons have focused on the spatial structure of receptive fields. For a more complete functional description of these neurons, it is necessary to consider receptive-field structure in the joint domain of space and time. We have studied the spatiotemporal receptive-field structure of 233 simple cells recorded from the striate cortex of adult cats and kittens at 4 and 8 wk postnatal. The dual goal of this study is to provide a detailed quantitative description of spatiotemporal receptive-field structure and to compare the developmental time courses of spatial and temporal response properties. 2. Spatiotemporal receptive-field profiles have been measured with the use of a reverse correlation method, in which we compute the cross-correlation between a neuron's response and a random sequence of small, briefly presented bright and dark stimuli. The receptive-field profiles of some simple cells are space-time separable, meaning that spatial and temporal response characteristics can be dissociated. Other cells have receptive-field profiles that are space-time inseparable. In these cases, a particular spatial location cannot be designated, unambiguously, as belonging to either an on or off subregion. However, separate on and off subregions may be clearly distinguished in the joint space-time domain. These subregions are generally tilted along an oblique axis. 3. Our observations show that spatial and temporal aspects of receptive-field structure mature with clearly different time courses. By 4 wk postnatal, the spatial symmetry and periodicity of simple-cell receptive fields have reached maturity. The spatial extent (or size) of these receptive fields is adult-like by 8 wk postnatal. In contrast, the response latency and time duration of spatiotemporal receptive fields do not mature until well beyond 8 wk postnatal. 4. By applying Fourier analysis to spatiotemporal receptive-field profiles, we have examined the postnatal development of spatial and temporal selectivity in the frequency domain. By 8 wk postnatal, spatial frequency tuning has clearly reached maturity. On the contrary, temporal frequency selectivity remains markedly immature at 8 wk. We have also examined the joint distribution of optimal spatial and temporal frequencies. From 4 wk postnatal until 8 wk postnatal, the range of optimal spatial frequencies increases substantially, whereas the range of optimal temporal frequencies remains largely unchanged. From 8 wk postnatal until adulthood, there is a large increase in optimal temporal frequencies for cells tuned to low spatial frequencies. For cells tuned to high spatial frequencies, the distribution of optimal temporal frequencies does not change much beyond 8 wk postnatal.(ABSTRACT TRUNCATED AT 400

title: Contrast invariance of functional maps in cat primary visual cortex.
abstract: Neurons in cat primary visual cortex (V1) are clustered according to their preference for stimulus position, orientation, spatial frequency, and eye of presentation, thereby giving rise to functional maps. It is not known, however, whether a similar arrangement is present for stimulus contrast. Neurons in cat V1 vary considerably in their contrast responses, and might be clustered in a systematic fashion in this respect. Additionally, stimulus contrast might affect other functional maps. For example, there has been debate over whether the contrast threshold of neurons in cytochrome oxidase blobs is lower than elsewhere. Here we have imaged intrinsic signals to measure orientation maps in cat V1 at a range of contrast levels. We determined, on a pixel-by-pixel basis, contrast-response functions and orientation tuning curves. The fit parameters describing contrast responses were more or less uniform: We found no regions where neurons have lower contrast threshold than elsewhere. If such regions do exist, their functional maps must be substantially weaker than maps of orientation preference. Moreover, we found that contrast has no impact on maps of orientation preference: The orientation selectivity of each pixel is invariant with stimulus contrast. The contrast invariance that we demonstrate at the level of maps is well known at the level of single neurons. It suggests that neurons contributing to a pixel response generally have similar orientation preferences or similar contrast responses. The latter explanation is likely to hold in pinwheel centers, where preferred orientation of nearby neurons can differ markedly. In summary, our data suggest that contrast is represented uniformly over the surface of cat V1, and changes in contrast do not affect maps of orientation preference.

title: Dynamics of Spatial Frequency Tuning in Macaque V1
abstract: Spatial frequency tuning in the lateral geniculate nucleus of the thalamus (LGN) and primary visual cortex (V1) differ substantially. LGN responses are largely low-pass in spatial frequency, whereas the majority of V1 neurons have bandpass characteristics. To study this transformation in spatial selectivity, we measured the dynamics of spatial frequency tuning using a reverse correlation technique. We find that a large proportion of V1 cells show inseparable responses in spatial frequency and time. In several cases, tuning becomes more selective over the course of the response, and the preferred spatial frequency shifts from low to higher frequencies. Many responses also show suppression at low spatial frequencies, which correlates with the increases in response selectivity and the shifts of preferred spatial frequency. These results indicate that suppression plays an important role in the generation of bandpass selectivity in V1.

title: Spatial frequency and orientation tuning dynamics in area V1
abstract: Spatial frequency (SF) and orientation tuning are intrinsic properties of neurons in primary visual cortex (area V1). To investigate the neural mechanisms mediating selectivity in the awake animal, we measured the temporal dynamics of SF and orientation tuning. We adapted a high-speed reverse-correlation method previously used to characterize orientation tuning dynamics in anesthetized animals to estimate efficiently the complete spatiotemporal receptive fields in area V1 of behaving macaques. We found that SF and orientation tuning are largely separable over time in single neurons. However, spatiotemporal receptive fields also contain a small nonseparable component that reflects a significant difference in response latency for low and high SF stimuli. The observed relationship between stimulus SF and latency represents a dynamic shift in SF tuning, and suggests that single V1 neurons might receive convergent input from the magno- and parvocellular processing streams. Although previous studies with anesthetized animals suggested that orientation tuning could change dramatically over time, we find no substantial evidence of dynamic changes in orientation tuning.

title: Visual cortex neurons in monkey and cat: effect of contrast on the spatial and temporal phase transfer functions.
abstract: The responses of simple cells (recorded from within the striate visual cortex) were measured as a function of the contrast and the frequency of sine-wave grating patterns in order to explore the effect of contrast on the spatial and temporal phase transfer functions and on the spatiotemporal receptive field. In general, as the contrast increased, the phase of the response advanced by approximately 45 ms (approximately one-quarter of a cycle for frequencies near 5 Hz), although the exact value varied from cell to cell. The dynamics of this phase-advance were similar to the dynamics of the amplitude: the amplitude and the phase increased in an accelerating fashion at lower contrasts and then saturated at higher contrasts. Further, the gain for both the amplitude and the phase appeared to be governed by the magnitude of the contrast rather than the magnitude of the response. For the spatial phase transfer function, variations in contrast had little or no systematic effect; all of the phase responses clustered around a single straight line, with a common slope and intercept. This implies that the phase-advance was not due to a change in the spatial properties of the neuron; it also implies that the phase-advance was not systematically related to the magnitude of the response amplitude. On the other hand, for the temporal phase transfer function, the phase responses fell on five straight lines, related to the five steps in contrast. As the contrast increased, the phase responses advanced such that both the slope and the intercept were affected. This implies that the phase-advance was a result of contrast-induced changes in both the response latency and the shape/symmetry of the temporal receptive field.

title: Summation and division by neurons in primate visual cortex.
abstract: Recordings from monkey primary visual cortex (V1) were used to test a model for the visually driven responses of simple cells. According to the model, simple cells compute a linear sum of the responses of lateral geniculate nucleus (LGN) neurons. In addition, each simple cell's linear response is divided by the pooled activity of a large number of other simple cells. The cell membrane performs both operations; synaptic currents are summed and then divided by the total membrane conductance. Current and conductance are decoupled (by a complementary arrangement of excitation and inhibition) so that current depends only on the LGN inputs and conductance depends only on the cortical inputs. Closed form expressions were derived for fitting and interpreting physiological data. The model accurately predicted responses to drifting grating stimuli of various contrasts, orientations, and spatiotemporal frequencies.

title: Temporal precision in the neural code and the timescales of natural vision
abstract: The timing of action potentials relative to sensory stimuli can be precise down to milliseconds in the visual system, even though the relevant timescales of natural vision are much slower. The existence of such precision contributes to a fundamental debate over the basis of the neural code and, specifically, what timescales are important for neural computation. Using recordings in the lateral geniculate nucleus, here we demonstrate that the relevant timescale of neuronal spike trains depends on the frequency content of the visual stimulus, and that ‘relative’, not absolute, precision is maintained both during spatially uniform white-noise visual stimuli and naturalistic movies. Using information-theoretic techniques, we demonstrate a clear role of relative precision, and show that the experimentally observed temporal structure in the neuronal response is necessary to represent accurately the more slowly changing visual world. By establishing a functional role of precision, we link visual neuron function on slow timescales to temporal structure in the response at faster timescales, and uncover a straightforward purpose of fine-timescale features of neuronal spike trains.

title: Gamma oscillation maintains stimulus structure-dependent synchronization in cat visual cortex.
abstract: Visual cortical cells demonstrate both oscillation and synchronization, although the underlying causes and functional significance of these behaviors remain uncertain. We simultaneously recorded single-unit activity with microelectrode arrays in supragranular layers of area 17 of cats paralyzed and anesthetized with propofol and N(2)O. Rate-normalized autocorrelograms of 24 cells reveal bursting (100%) and gamma oscillation (63%). Renewal density analysis, used to explore the source of oscillation, suggests a contribution from extrinsic influences such as feedback. However, a bursting refractory period, presumably membrane-based, could also encourage oscillatory firing. When we investigated the source of synchronization for 60 cell pairs we found only moderate correlation of synchrony with bursts and oscillation. We did, nonetheless, discover a possible functional role for oscillation. In all cases of cross-correlograms that exhibited oscillation, the strength of the synchrony was maintained throughout the stimulation period. When no oscillation was apparent, 75% of the cell pairs showed decay in their synchronization. The synchrony between cells is strongly dependent on similar response onset latencies. We therefore propose that structured input, which yields tight organization of latency, is a more likely candidate for the source of synchronization than oscillation. The reliable synchrony at response onset could be driven by spatial and temporal correlation of the stimulus that is preserved through the earlier stages of the visual system. Oscillation then contributes to maintenance of the synchrony to enhance reliable transmission of the information for higher cognitive processing.

title: Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex
abstract: Simple cells in the primary visual cortex often appear to compute a weighted sum of the light intensity distribution of the visual stimuli that fall on their receptive fields. A linear model of these cells has the advantage of simplicity and captures a number of basic aspects of cell function. It, however, fails to account for important response nonlinearities, such as the decrease in response gain and latency observed at high contrasts and the effects of masking by stimuli that fail to elicit responses when presented alone. To account for these nonlinearities we have proposed a normalization model, which extends the linear model to include mutual shunting inhibition among a large number of cortical cells. Shunting inhibition is divisive, and its effect in the model is to normalize the linear responses by a measure of stimulus energy. To test this model we performed extracellular recordings of simple cells in the primary visual cortex of anesthetized macaques. We presented large stimulus sets consisting of (1) drifting gratings of various orientations and spatiotemporal frequencies; (2) plaids composed of two drifting gratings; and (3) gratings masked by full-screen spatiotemporal white noise. We derived expressions for the model predictions and fitted them to the physiological data. Our results support the normalization model, which accounts for both the linear and the nonlinear properties of the cells. An alternative model, in which the linear responses are subject to a compressive nonlinearity, did not perform nearly as well.

title: Normalization of cell responses in cat striate cortex.
abstract: Simple cells in the striate cortex have been depicted as half-wave-rectified linear operators. Complex cells have been depicted as energy mechanisms, constructed from the squared sum of the outputs of quadrature pairs of linear operators. However, the linear/energy model falls short of a complete explanation of striate cell responses. In this paper, a modified version of the linear/energy model is presented in which striate cells mutually inhibit one another, effectively normalizing their responses with respect to stimulus contrast. This paper reviews experimental measurements of striate cell responses, and shows that the new model explains a significantly larger body of physiological data.

title: Complex Dynamics of V1 Population Responses Explained by a Simple Gain-Control Model
abstract: To understand sensory encoding and decoding, it is essential to characterize the dynamics of population responses in sensory cortical areas. Using voltage-sensitive dye imaging in awake, fixating monkeys, we obtained complete quantitative measurements of the spatiotemporal dynamics of V1 responses over the entire region activated by small, briefly presented stimuli. The responses exhibit several complex properties: they begin to rise approximately simultaneously over the entire active region, but reach their peak more rapidly at the center. However, at stimulus offset the responses fall simultaneously and at the same rate at all locations. Although response onset depends on stimulus contrast, both the peak spatial profile and the offset dynamics are independent of contrast. We show that these results are consistent with a simple population gain-control model that generalizes earlier single-neuron contrast gain-control models. This model provides valuable insight and is likely to be applicable to other brain areas.

title: A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex
abstract: Cortical synapses exhibit several forms of short-term plasticity, but the contribution of this plasticity to visual response dynamics is unknown. In part, this is because the simple patterns of stimulation used to probe plasticity in vitro do not correspond to patterns of activity that occur in vivo. We have developed a method of quantitatively characterizing short-term plasticity at cortical synapses that permits prediction of responses to arbitrary patterns of stimulation. Synaptic responses were recorded intracellularly as EPSCs and extracellularly as local field potentials in layer 2/3 of rat primary visual cortical slices during stimulation of layer 4 with trains of electrical stimuli containing random mixtures of frequencies. Responses exhibited complex dynamics that were well described by a simple three-component model consisting of facilitation and two forms of depression, a stronger form that decayed exponentially with a time constant of several hundred milliseconds and a weaker, but more persistent, form that decayed with a time constant of several seconds. Parameters obtained from fits to one train were used to predict accurately responses to other random and constant frequency trains. Control experiments revealed that depression was not caused by a decrease in the effectiveness of extracellular stimulation or by a buildup of inhibition. Pharmacological manipulations of transmitter release and postsynaptic sensitivity suggested that both forms of depression are mediated presynaptically. These results indicate that firing evoked by visual stimuli is likely to cause significant depression at cortical synapses. Hence synaptic depression may be an important determinant of the temporal features of visual cortical responses.

title: Functional Mechanisms Shaping Lateral Geniculate Responses to Artificial and Natural Stimuli
abstract: Functional models of the early visual system should predict responses not only to simple artificial stimuli but also to sequences of complex natural scenes. An ideal testbed for such models is the lateral geniculate nucleus (LGN). Mechanisms shaping LGN responses include the linear receptive field and two fast adaptation processes, sensitive to luminance and contrast. We propose a compact functional model for these mechanisms that operates on sequences of arbitrary images. With the same parameters that fit the firing rate responses to simple stimuli, it predicts the bulk of the firing rate responses to complex stimuli, including natural scenes. Further improvements could result by adding a spiking mechanism, possibly one capable of bursts, but not by adding mechanisms of slow adaptation. We conclude that up to the LGN the responses to natural scenes can be largely explained through insights gained with simple artificial stimuli.

title: Asymmetric synaptic depression in cortical networks.
abstract: Synaptic depression is essential for controlling the balance between excitation and inhibition in cortical networks. Several studies have shown that the depression of intracortical synapses is asymmetric, that is, inhibitory synapses depress less than excitatory ones. Whether this asymmetry has any impact on cortical function is unknown. Here we show that the differential depression of intracortical synapses provides a mechanism through which the gain and sensitivity of cortical circuits shifts over time to improve stimulus coding. We examined the functional consequences of asymmetric synaptic depression by modeling recurrent interactions between orientation-selective neurons in primary visual cortex (V1) that adapt to feedforward inputs. We demonstrate analytically that despite the fact that excitatory synapses depress more than inhibitory synapses, excitatory responses are reduced less than inhibitory ones to increase the overall response gain. These changes play an active role in generating selective gain control in visual cortical circuits. Specifically, asymmetric synaptic depression regulates network selectivity by amplifying responses and sensitivity of V1 neurons to infrequent stimuli and attenuating responses and sensitivity to frequent stimuli, as is indeed observed experimentally.

title: Stimulus contrast modulates functional connectivity in visual cortex
abstract: Neurons in visual cortex are linked by an extensive network of lateral connections. To study the effect of these connections on neural responses, we recorded spikes and local field potentials (LFPs) from multi-electrode arrays that were implanted in monkey and cat primary visual cortex. Spikes at each location generated outward traveling LFP waves. When the visual stimulus was absent or had low contrast, these LFP waves had large amplitudes and traveled over long distances. Their effect was strong: LFP traces at any site could be predicted by the superposition of waves that were evoked by spiking in a ∼1.5-mm radius. As stimulus contrast increased, both the magnitude and the distance traveled by the waves progressively decreased. We conclude that the relative weight of feedforward and lateral inputs in visual cortex is not fixed, but rather depends on stimulus contrast. Lateral connections dominate at low contrast, when spatial integration of signals is perhaps most beneficial.

title: The Correlation Theory of Brain Function
abstract: A summary of brain theory is given so far as it is contained within the framework of Localization Theory. Diffculties of this "conventional theory" are traced back to a specific deficiency: there is no way to express relations between active cells (as for instance their representing parts of the same object). A new theory is proposed to cure this deficiency. It introduces a new kind of dynamical control, termed synaptic modulation, according to which synapses switch between a conducting and a non- conducting state. The dynamics of this variable is controlled on a fast time scale by correlations in the temporal fine structure of cellular signals. Furthermore, conventional synaptic plasticity is replaced by a refined version. Synaptic modulation and plasticity form the basis for short-term and long-term memory, respectively. Signal correlations, shaped by the variable network, express structure and relationships within objects. In particular, the figure-ground problem may be solved in this way. Synaptic modulation introduces flexibility into cerebral networks which is necessary to solve the invariance problem. Since momentarily useless connections are deactivated, interference between different memory traces can be reduced, and memory capacity increased, in comparison with conventional associative memory.

title: Adaptation to Stimulus Contrast and Correlations during Natural Visual Stimulation
abstract: In this study, we characterize the adaptation of neurons in the cat lateral geniculate nucleus to changes in stimulus contrast and correlations. By comparing responses to high- and low-contrast natural scene movie and white noise stimuli, we show that an increase in contrast or correlations results in receptive fields with faster temporal dynamics and stronger antagonistic surrounds, as well as decreases in gain and selectivity. We also observe contrast- and correlation-induced changes in the reliability and sparseness of neural responses. We find that reliability is determined primarily by processing in the receptive field (the effective contrast of the stimulus), while sparseness is determined by the interactions between several functional properties. These results reveal a number of adaptive phenomena and suggest that adaptation to stimulus contrast and correlations may play an important role in visual coding in a dynamic natural environment.

title: How is direction selectivity organized in the extrastriate visual area PMLS of the cat?
abstract: Although most neurones in the PMLS of the cat are selective for direction of motion, whether the preferred directions are organized into cortical columns, as they are in the MT area of the monkey, is not certain. We have quantitatively investigated the organization of direction selectivity of PMLS neurones. The results showed that adjacent neurones have similar direction selectivity. The preferred direction of neurones sampled successively in a tangential penetration changed continually, occasionally with an approximately 180 degrees reversal, and neurones with bidirectional selectivity tended to be located in the reversal region. It is spectulated that direction selectivity in the PMLS is organized on the basis of preferred axis of motion in such a way that one column with bidirectional preference lies between two columns with opposite unidirectional preferences, a unidirectional column is always adjacent to a bidirectional column and these adjacent columns share a common preferred axis-of-motion.

title: Representation of surface luminance and contrast in primary visual cortex.
abstract: In visual perception, object identification requires both the ability to define regions of uniform luminance and zones of luminance contrast. Neural processes underlying contrast detection have been well studied, while those defining luminance remain poorly understood and controversial. Partially because stimuli comprised of uniform luminance are relatively ineffective in driving responses of cortical neurons, little effort has been made to systematically compare responses of individual neurons to both uniform luminance and contrast. Using large static uniform luminance and contrast stimuli, modulated temporally in luminance or contrast, we found a continuum of responses ranging from a few cells modulated only by luminance (luminance-only), to many cells modulated by both luminance and contrast (luminance-contrast), and to many others modulated only by contrast (contrast-only) in primary visual cortex. Moreover, luminance-contrast cells had broader orientation tuning, larger receptive field (RF) and lower spatial frequency Preference, on average, than contrast-only cells. Contrast-only cells had contrast responses more linearly correlated to the spatial structure of their RFs than luminance-contrast cells. Taken together these results suggest that luminance and contrast are represented, to some degree, by independent mechanisms that may be shaped by different classes of subcortical and/or cortical inputs.

title: Dynamics of orientation tuning in macaque primary visual cortex
abstract: Orientation tuning of neurons is one of the chief emergent characteristics of the primary visual cortex, VI (refs 1,2). Neurons of the lateral geniculate nucleus, which comprise the thalamic input to VI, are not orientation-tuned, but the majority of VI neurons are quite selective. How orientation tuning arises within VI is still controversial1,3–17. To study this problem, we measured how the orientation tuning of neurons evolves with time18–20 using a new method: reverse correlation in the orientation domain. Orientation tuning develops after a delay of 30–45 milliseconds and persists for 40–85 ms. Neurons in layers 4Cα or 4Cβ, which receive direct input from the thalamus, show a single orientation preference which remains unchanged throughout the response period. In contrast, the preferred orientations of output layer neurons (in layers 2,3,4B, 5 or 6) usually change with time, and in many cases the orientation tuning may have more than one peak. This difference in dynamics is accompanied by a change in the sharpness of orientation tuning; cells in the input layers are more broadly tuned than cells in the output layers. Many of these observed properties of output layer neurons cannot be explained by simple feedforward models1,3–6, whereas they arise naturally in feedback networks7–17. Our results indicate that VI is more than a bank of static oriented filters; the dynamics of output layer cells appear to be shaped by intracortical feedback.

title: Accuracy of subspace mapping of spatiotemporal frequency domain visual receptive fields.
abstract: Orientation and spatial frequency selectivities are fundamental properties of cells in the early visual cortex. Although they are customarily tested with drifting sinusoidal gratings, a recently developed subspace reverse correlation method may be a better replacement for obtaining a selectivity map in a joint orientation and spatial frequency domain at higher resolution efficiently. These two methods are examined for their accuracy and data compatibility for cells in areas 17 and 18 of anesthetized and paralyzed cats. Peaks and bandwidths of tuning curves from these two methods are highly correlated. However, spatial frequency bandwidths obtained by reverse correlation tend to be slightly narrower for the subspace reverse correlation than those from the drifting grating tests. Consistency between the two methods is improved if the entire duration of data containing signal are taken into account for the subspace reverse correlation rather than using the map only at the optimal correlation delay. Examination of convergence of the subspace mapping process shows that reliable 2-day profiles can be obtained within 5-10 min. for the majority of cells. Temporal dynamics of tuning properties are also examined more directly with the subspace mapping than with the drifting gratings. For many cells, the optimal spatial frequency shifts substantially, measured as a fraction of tuning bandwidth, over the time course of response. In comparison, the optimal orientation remains highly stable throughout the duration of response. Overall, these results suggest that the subspace reverse correlation is a better substitute for the conventional method.

title: Classifying simple and complex cells on the basis of response modulation
abstract: Hubel and Wiesel (1962;  introduced the classification of cortical neurons as simple and complex on the basis of four tests of their receptive field structure. These tests are partly subjective and no one of them unequivocally places neurons into distinct classes. A simple, objective classification criterion based on the form of the response to drifting sinusoidal gratings has been used by several laboratories, although it has been criticized by others. We review published and unpublished evidence which indicates that this simple and objective criterion reliability divides neurons of the striate cortex in both cats and monkeys into two groups that correspond closely to the classically-described simple and complex classes.

title: Contrast adaptation and excitatory amino acid receptors in cat striate cortex.
abstract: We have employed two paradigms to investigate the mechanisms of contrast gain control in cat striate cortex. In the first paradigm, optimal drifting gratings were presented in three consecutive periods. The contrast was near threshold in the first and third periods and accompanied by iontophoretic pulses of glutamate or glutamate receptor (GluR) agonists. The contrast was set to evoke a higher firing rate in the second period. Although both visual and iontophoretic conditions were identical in the first and third periods, responses to glutamate, N-methyl-D-aspartic acid (NMDA), and (IS,3R)-1-Aminocyclopentane-1,3-dicarboxylic acid (ACPD) were reduced following the adapting interval. (S)-alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) responses were not reduced. Administration of ionotropic GluR antagonists did not affect adaptation to the high-contrast grating. The metabotropic GluR antagonist (+/-)-alpha-Methyl-4-carboxyphenylglycine (MCPG), which acts at presynaptic glutamate autoreceptors, decreased the degree of adaptation exhibited by striate cells. In a second paradigm, contrast response functions (CRFs) were obtained at various adapting contrasts and least-squares fits to a hyperbolic ratio equation generated for each adapting level. Similar to previous reports, DL-2-amino-5-phosphonovaleric acid (APV) reduced the slope of the CRF and increased the responsiveness of the cells but did not affect the semisaturation constant, sigma, or the exponent of the CRF, n. Only MCPG significantly altered the distribution of sigma and n for 19 cells. The effect on sigma suggests that this drug can interfere with the cell's ability to shift its operating point to match the adapting contrast. These results suggest the involvement of a presynaptic mechanism for contrast adaptation. The decrease in neuronal responsiveness immediately following the high-contrast period may reflect an additional, postsynaptic effect in which there is a decrease in the NMDA-mediated component of the visual response.

title: Contrast normalization and a linear model for the directional selectivity of simple cells in cat striate cortex.
abstract: Previous tests of the linearity of spatiotemporal summation in cat simple cells have compared the responses to moving sinusoidal gratings and to gratings whose contrast was modulated sinusoidally in time. In particular, since a moving grating can be expressed as a sum of modulated gratings, the response to a moving grating should be predictable (assuming linearity) from the responses to modulated gratings. However, these simple linear predictions have shown varying degrees of failure (e.g. Reid et al., 1987, 1991), depending on the directional selectivity of the neurons (Tolhurst & Dean, 1991). We demonstrate here that the failures of these linear predictions are, in fact, explained by the contrast-normalization model of Heeger (1993). We concentrate on the ratio of the measured to predicted moving grating responses. In the context of the contrast-normalization model, calculating this ratio turns out to be particularly appropriate, since the ratio is independent of the precise details of the linear front-end mechanisms ultimately responsible for directional selectivity. Hence, the contrast-normalization model can be compared quantitatively with this ratio measure, by varying only one free parameter. When account is taken both of the expansive output nonlinearity and of contrast normalization, the directional selectivity of simple cells seems to be dependent only on linear spatiotemporal filtering.