Contrast adaptation is spatial frequency specific in mouse primary visual cortex.

Contrast adaptation, generated by prolonged viewing of a high contrast spatial pattern, is known to reduce perceptual sensitivity to subsequently presented stimuli of similar spatial frequency (SF). Neural correlates of this pattern-specific contrast adaptation have been described in several classic studies in cat primary visual cortex (V1). These results have also recently been extended to mice, which is a genetically manipulable animal model. Here we attempt to parse the potential mechanisms contributing to this phenomenon by determining whether the SF specificity of contrast adaptation observed in mouse V1 neurons depends on the spike rate elicited by the adapting gratings. We found that adapting stimuli that drove a neuron more strongly generally produced more adaptation, implicating an intrinsic or fatigue-like process. Importantly, we also observed that slightly stronger contrast adaptation was produced when the adapting SF matched the test SF even when matched and nonmatched adapting gratings elicited similar spike rates indicating extrinsic or network processes contribute as well.

Spatiotemporal tuning in mouse primary visual cortex.

The neural correlates of visual motion perception have historically been studied in non-human primates. However, the mouse has recently gained popularity as a model for studying vision primarily driven by the hope that the genetic tools available in this species may contribute to our understanding of visual processing in the cortex. A recent calcium-imaging study on the spatiotemporal tuning of mouse striate and extrastriate cortex revealed that neurons in the primary visual cortex (V1) were almost never speed tuned, whereas previous electrophysiological studies in macaques noted around one quarter of V1 neurons appeared to be selective for a particular stimulus speed. We were interested in whether this discrepancy was due to methodological or species differences, so we measured the spatiotemporal tuning of mouse V1 neurons using standard electrophysiological techniques. Using comparable analyses to previous studies of speed tuning, our data showed that speed tuning is rare in mouse V1, which corroborates earlier studies in mouse and points to a species difference in motion processing in early cortex between macaques and other mammals.

Dynamic contrast change produces rapid gain control in visual cortex.

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.

Influence of adapting speed on speed and contrast coding in the primary visual cortex of the cat.

Adaptation is a ubiquitous property of the visual system. Adaptation often improves the ability to discriminate between stimuli and increases the operating range of the system, but is also associated with a reduced ability to veridically code stimulus attributes. Adaptation to luminance levels, contrast, orientation, direction and spatial frequency has been studied extensively, but knowledge about adaptation to image speed is less well understood. Here we examined how the speed tuning of neurons in cat primary visual cortex was altered after adaptation to speeds that were slow, optimal, or fast relative to each neuron's speed response function. We found that the preferred speed (defined as the speed eliciting the peak firing rate) of the neurons following adaptation was dependent on the speed at which they were adapted. At the population level cells showed decreases in preferred speed following adaptation to speeds at or above the non-adapted speed, but the preferred speed did not change following adaptation to speeds lower than the non-adapted peak. Almost all cells showed response gain control (reductions in absolute firing capacity) following speed adaptation. We also investigated the speed dependence of contrast adaptation and found that most cells showed contrast gain control (rightward shifts of their contrast response functions) and response gain control following adaptation at any speed. We conclude that contrast adaptation may produce the response gain control associated with speed adaptation, but shifts in preferred speed require an additional level of processing beyond contrast adaptation. A simple model is presented that is able to capture most of the findings.

Complex cells increase their phase sensitivity at low contrasts and following adaptation.

One of the best-known dichotomies in neuroscience is the division of neurons in the mammalian primary visual cortex into simple and complex cells. Simple cells have receptive fields with separate on and off subregions and give phase-sensitive responses to moving gratings, whereas complex cells have uniform receptive fields and are phase invariant. The phase sensitivity of a cell is calculated as the ratio of the first Fourier coefficient (F1) to the mean time-average (Fo) of the response to moving sinusoidal gratings at 100% contrast. Cells are then classified as simple (F1/Fo >1) or complex (F1/Fo <1). We manipulated cell responses by changing the stimulus contrast or through adaptation. The F(1)/F(0) ratios of cells defined as complex at 100% contrast increased at low contrasts and following adaptation. Conversely, the F1/Fo ratios remained constant for cells defined as simple at 100% contrast. The latter cell type was primarily located in thalamorecipient layers 4 and 6. Many cells initially classified as complex exhibit F1/Fo >1 at low contrasts and after adaptation (particularly in layer 4). The results are consistent with the spike-threshold hypothesis, which suggests that the division of cells into two types arises from the nonlinear interaction of spike threshold with membrane potential responses.

Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex.

The responses of neurons in the middle temporal and medial superior temporal areas of macaque cortex are suppressed during saccades compared with saccade-like stimulus movements. We utilized the short-latency ocular following paradigm to show that this saccadic suppression is followed by postsaccadic enhancement of motion responses. The level of enhancement decays with a time constant of 100 ms from saccade end. The speed of ocular following is also enhanced after saccades and decays over a similar time course, suggesting a link between the neural and behavioral effects. There is some evidence that maximum postsaccadic enhancement occurs when cells are stimulated at their optimum speeds. Latencies of motion responses are saccade dependent: 37 ms for saccade-generated motion, 45 ms for motion in the half-second after saccades, and 70 ms with no prior saccades. The finding that saccades alter response latencies may partially explain perceptual time compression during saccades and time dilation after saccades.

Contrast gain control is drift-rate dependent: an informational analysis.

Neurons in the visual cortex code relative changes in illumination (contrast) and adapt their sensitivities to the visual scene by centering the steepest regions of their sigmoidal contrast response functions (CRFs: spike rate as a function of contrast) on the prevailing contrast. The influence of this contrast gain control has not been reported at nonoptimal drift rates. We calculated the Fisher information contained in the CRFs of halothane-anesthetized cats. Fisher information gives a measure of the accuracy of contrast representations based on the ratio of the square of the steepness of the CRF and the spike-rate dependency of the spiking variance. Variance increases with spike rate, so Fisher information is maximal where the CRF is steep and spike rates are low. Here, we show that the contrast at which the maximal Fisher information (C(MFI)) occurs for each adapting drift rate is at a fixed level above the adapting contrast. For adapting contrasts of 0 to 0.32 the relationship between C(MFI) and adapting contrast is well described by a straight line with a slope close to 1. The intercept of this line on the C(MFI)-axis is drift-rate dependent, although the slope is not. At high drift rates relative to each cell's peak the C(MFI) offset is higher than that for low drift rates. The results show that the contrast coding strategy in visual cortex maximizes accuracy for contrasts above the prevailing contrast in the environment for all drift rates. We argue that tuning the system for accuracy at contrasts above the prevailing value is optimal for viewing natural scenes.

Neurons in V1, V2, and PMLS of cat cortex are speed tuned but not acceleration tuned: the influence of motion adaptation.

We studied neurons in areas V1, V2, and posteromedial lateral suprasylvian area (PMLS) of anesthetized cats, assessing their speed tuning using steps to constant speeds and acceleration and deceleration tuning using speed ramps. The results show that the speed tuning of neurons in all three cortical areas is highly dependent on prior motion history, with early responses during speed steps tuned to higher speeds than later responses. The responses to speed ramps are profoundly influenced by speed-dependent response latencies and ongoing changes in neuronal speed tuning due to adaptation. Acceleration evokes larger transient and sustained responses than subsequent deceleration of the same rate with this disparity increasing with ramp rate. Consequently, there was little correlation between preferred speeds measured using speed steps, acceleration or deceleration. From 146 recorded cells, the proportion of cells that were clearly speed tuned ranged from 69 to 100% across the three brain areas. However, only 13 cells showed good skewed Gaussian fits and systematic variation in their responses to a range of accelerations. Although suggestive of acceleration coding, this apparent tuning was attributable to a cell's speed tuning and the different stimulus durations at each acceleration rate. Thus while the majority of cells showed speed tuning, none unequivocally showed acceleration tuning. The results are largely consistent with an existing model that predicts responses to accelerating stimuli developed for macaque MT, which showed that the responses to acceleration can be decoded if adaptation is taken into account. However, the present results suggest future models should include stimulus-specific adaptation and speed-dependent response latencies.

Relationship between contrast adaptation and orientation tuning in V1 and V2 of cat visual cortex.

Previous studies investigating the response properties of neurons in the primary visual cortex of cats and primates have shown that prolonged exposure to optimally oriented, high-contrast gratings leads to a reduction in responsiveness to subsequently presented test stimuli. We recorded from 119 neurons in cat V1 and V2 and found that in a high proportion of cells contrast adaptation also occurs for gratings oriented orthogonal to a neuron's preferred orientation, even though this stimulus did not elicit significant increases in spiking activity. Approximately 20% of neurons adapted equally to all orientations tested and a further 46% showed at least some adaptation to orthogonally oriented gratings, whereas 20% of neurons did not adapt to orthogonal gratings. The magnitude of contrast adaptation was positively correlated with adapting contrast, but was not related to the spiking activity of the cells. Highly direction selective neurons produced stronger adaptation to orthogonally oriented gratings than other neurons. Orientation-related adaptation was correlated with the rate of change of orientation tuning in consecutive cells along electrode penetrations that traveled parallel to the cortical layers. Nonoriented adaptation was most common in areas where orientation preference changed rapidly, whereas orientation-selective adaptation was most common in areas where orientation preference changed slowly. A minority of neurons did not show contrast adaptation (14%). No major differences were found between units in different cortical layers, V1 and V2, or between complex and simple cells. The relevance of these findings to the current understanding of adaptation within the context of orientation column architecture is discussed.

On the division of cortical cells into simple and complex types: a comparative viewpoint.

Hubel and Weisel introduced the concept of cells in cat primary visual cortex being partitioned into two categories: simple and complex. Subsequent authors have developed a quantitative measure to distinguish the two cell types based on the ratio between modulated responses at the stimulus frequency (F1) and unmodulated (F0) components of the spiking responses to drifting sinusoidal gratings. It has been shown that cells in anesthetized cat and monkey cortex have bimodal distributions of F1/F0 ratios. A clear local minimum or dip exists in the distribution at a ratio close to unity. Here we present a comparison of the distributions of the F1/F0 ratios between cells in the primary visual cortex of the eutherian cat and marsupial Tammar wallaby, Macropus eugenii. This is the first quantitative description of any marsupial cortex using the F1/F0 ratio and follows earlier papers showing that cells in wallaby cortex are tightly oriented and spatial frequency tuned. The results reveal a bimodal distribution in the wallaby F1/F0 ratios that is very similar to that found in the rat, cat, and monkey. Discussion focuses on the mechanisms that could lead to such similar cell distributions in animals with diverse behaviors and phylogenies.

Fast and slow neurons in the nucleus of the basal optic root in pigeons.

The nucleus of the basal optic root (nBOR) is involved in the generation of the optokinetic response. Previous studies showed that most nBOR neurons exhibit direction-selectivity in response to largefield motion. We investigated the responses of pigeon nBOR neurons to drifting sine wave gratings of varying spatial and temporal frequency (SF,TF). Two groups of neurons were revealed. The first group preferred gratings of low SF (mean, 0.07 cycles per degree (cpd)) and high TF (mean, 0.76 Hz) ('fast' stimuli). The second group preferred gratings of high SF (mean, 0.56 cpd) and lower TF (mean, 0.33 Hz) ('slow' stimuli). Previous studies have demonstrated fast and slow neurons in pretectal nucleus lentiformis mesencephali, which is also involved in the generation of the optokinetic response.

Spatiotemporal properties of fast and slow neurons in the pretectal nucleus lentiformis mesencephali in pigeons.

Neurons in the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow that results from self-motion. Previous studies have shown that LM neurons have large receptive fields in the contralateral eye, are excited in response to largefield stimuli moving in a particular (preferred) direction, and are inhibited in response to motion in the opposite (anti-preferred) direction. We investigated the responses of LM neurons to sine wave gratings of varying spatial and temporal frequency drifting in the preferred and anti-preferred directions. The LM neurons fell into two categories. "Fast" neurons were maximally excited by gratings of low spatial [0.03-0.25 cycles/ degrees (cpd)] and mid-high temporal frequencies (0.5-16 Hz). "Slow" neurons were maximally excited by gratings of high spatial (0.35-2 cpd) and low-mid temporal frequencies (0.125-2 Hz). Of the slow neurons, all but one preferred forward (temporal to nasal) motion. The fast group included neurons that preferred forward, backward, upward, and downward motion. For most cells (81%), the spatial and temporal frequency that elicited maximal excitation to motion in the preferred direction did not coincide with the spatial and temporal frequency that elicited maximal inhibition to gratings moving in the anti-preferred direction. With respect to motion in the anti-preferred direction, a substantial proportion of the LM neurons (32%) showed bi-directional responses. That is, the spatiotemporal plots contained domains of excitation in addition to the region of inhibition. Neurons tuned to stimulus velocity across different spatial frequency were rare (5%), but some neurons (39%) were tuned to temporal frequency. These results are discussed in relation to previous studies of the responses of neurons in the accessory optic system and pretectum to drifting gratings and other largefield stimuli.

Topographic organization of inferior olive cells projecting to translational zones in the vestibulocerebellum of pigeons.

In the nodulus and ventral uvula of pigeons, there are four parasagittal zones containing Purkinje cells responsive to patterns of optic flow that results from self-translation along a particular axis in three-dimensional space. By using a three-axis system to describe the preferred direction of translational optic flow, where +X, +Y, and +Z represent rightward, upward, and forward self-motion, respectively, the four cell types are: +Y, -Y, -X-Z, and -X+Z (assuming recording from the left side of the head). The -X-Z zone is the most medial, followed in sequence by the -X+Z, -Y zone, and the +Y zones. In this study, we injected the retrograde tracer cholera toxin subunit B into each of the four translational zones to determine the origin of the climbing fiber inputs in the inferior olive. Retrograde labeling in the inferior olive was found in the ventrolateral margin of the medial column from injections into all four translational zones; however, there was a clear functional topography. Retrograde labeling from -Y zone injections was found most rostrally in the medial column, whereas retrogradely labeled cells from -X-Z zone injections were found most caudally in the medial column. Labeling from +Y and -X+Z zone injections were found between the labeling from -Y zones and -X-Z zones, with +Y labeling located slightly caudal to -X+Z labeling.