Markus Hietanen

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 neurons 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.

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.

Differential changes in human perception of speed due to motion adaptation.

Visual systems adapt to the prevailing image conditions. This improves the ability to discriminate between two similar stimuli but has the side effect that veridical perception is degraded. For example, prolonged driving at 100 km/h may reduce the perceived speed to 80 km/h but improve the sensitivity to changes in the prevailing speed. Here we use radially expanding flow fields with a wide combination of adapt and test speeds to study human speed perception. Adaptation at speeds higher than the test always attenuates perceived speed, whereas adaptation at low and testing at high speeds increases perceived speed. We show that adaptation is stronger (i.e., post-adaptation speeds are perceived as slower) when the dots in the expanding flow field accelerate towards the periphery rather than traveling at constant speeds. We also show that speed discriminability is reduced following adaptation to low speeds when tested at high speeds and increased when the test speed is at or below prior adaptation speeds. We conclude that the relative speeds of the adaptation and test patterns are important parameters governing speed-related adaptation effects in the human brain.

Sensory experience modifies feature map relationships in visual cortex

The extent to which brain structure is influenced by sensory input during development is a critical but controversial question. A paradigmatic system for studying this is the mammalian visual cortex. Maps of orientation preference (OP) and ocular dominance (OD) in the primary visual cortex of ferrets, cats and monkeys can be individually changed by altered visual input. However, the spatial relationship between OP and OD maps has appeared immutable. Using a computational model we predicted that biasing the visual input to orthogonal orientation in the two eyes should cause a shift of OP pinwheels towards the border of OD columns. We then confirmed this prediction by rearing cats wearing orthogonally oriented cylindrical lenses over each eye. Thus, the spatial relationship between OP and OD maps can be modified by visual experience, revealing a previously unknown degree of brain plasticity in response to sensory input. DOI: http://dx.doi.org/10.7554/eLife.13911.001

Focal activation of primary visual cortex following supra-choroidal electrical stimulation of the retina: Intrinsic signal imaging and linear model analysis

We performed optical intrinsic signal imaging of cat primary visual cortex (Area 17 and 18) while delivering bipolar electrical stimulation to the retina by way of a supra-choroidal electrode array. Using a general linear model (GLM) analysis we identified statistically significant (p < 0.01) activation in a localized region of cortex following supra-threshold electrical stimulation at a single retinal locus. Our results: (1) demonstrate that intrinsic signal imaging combined with linear model analysis provides a powerful tool for assessing cortical responses to prosthetic stimulation, and (2) confirm that supra-choroidal electrical stimulation can achieve localized activation of the cortex consistent with focal activation of the retina.

Long-term sensorimotor adaptation in the ocular following system of primates

The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement.

Spatial phase sensitivity of complex cells in primary visual cortex depends on stimulus contrast

Neurons in primary visual cortex are classified as simple, which are phase sensitive, or complex, which are significantly less phase sensitive. Previously, we have used drifting gratings to show that the phase sensitivity of complex cells increases at low contrast and after contrast adaptation while that of simple cells remains the same at all contrasts (Cloherty SL, Ibbotson MR. J Neurophysiol 113: 434-444, 2015; Crowder NA, van Kleef J, Dreher B, Ibbotson MR. J Neurophysiol 98: 1155-1166, 2007; van Kleef JP, Cloherty SL, Ibbotson MR. J Physiol 588: 3457-3470, 2010). However, drifting gratings confound the influence of spatial and temporal summation, so here we have stimulated complex cells with gratings that are spatially stationary but continuously reverse the polarity of the contrast over time (contrast-reversing gratings). By varying the spatial phase and contrast of the gratings we aimed to establish whether the contrast-dependent phase sensitivity of complex cells results from changes in spatial or temporal processing or both. We found that most of the increase in phase sensitivity at low contrasts could be attributed to changes in the spatial phase sensitivities of complex cells. However, at low contrasts the complex cells did not develop the spatiotemporal response characteristics of simple cells, in which paired response peaks occur 180° out of phase in time and space. Complex cells that increased their spatial phase sensitivity at low contrasts were significantly overrepresented in the supragranular layers of cortex. We conclude that complex cells in supragranular layers of cat cortex have dynamic spatial summation properties and that the mechanisms underlying complex cell receptive fields differ between cortical layers.

Differential changes in perceived contrast following contrast adaptation in humans.

Perceived contrast is reduced after prolonged exposure to a textured pattern (contrast adaptation). The size of this effect is dependent on the relationship between the adapting contrast and the test contrast. It is generally accepted that the greatest reductions occur when the adapting contrast is much higher than the test contrast. Here this relationship was examined for a wide range of spatial frequencies. The results show that the effect of the adapt/test ratio on perceived contrast following contrast adaptation is highly spatial frequency dependent. At high spatial frequencies >1cpd perceived contrast was reduced for all adapting contrasts, which is consistent with other studies. However, at low spatial frequencies (<1cpd) the perceived contrast was actually above veridical perception when the adapting contrast was lower than the test contrast. This finding has not been previously reported and has important implications for models of contrast perception.

The relative contributions of global and local acceleration components on speed perception and discriminability following adaptation.

The perception of speed is dependent on the history of previously presented speeds. Adaptation to a given speed regularly results in a reduction of perceived speed and an increase in speed discriminability and in certain circumstances can result in an increase in perceived speed. In order to determine the relative contributions of the local and global speed components on perceived speed, this experiment used expanding dot flow fields with accelerating (global), decelerating (global) and mixed accelerating/decelerating (local) speed patterns. Profound decreases in perceived speed are found when viewing low test speeds after adaptation to high speeds. Small increases in the perceived speed of high test speeds occur following adaptation to low speeds. There were small but significant differences in perceived stimulus speed after adaptation due to different acceleration profiles. No evidence for global modulation of speed discriminability following adaptation was found.

Contrast and response gain control depend on cortical map architecture

Visual cortical neurons are sensitive to visual stimulus contrast and most cells adapt their sensitivity to the prevailing visual environment. Specifically, they match the steepest region of their contrast response function to the prevailing contrast (contrast gain control), and reduce spike rates to limit saturation (response gain control). Most neurons are also tuned for stimulus orientation, and neurons with similar orientation preference are clustered together into iso‐orientation zones arranged around pinwheels, i.e. points where all orientations are represented. Here we investigated the relationship between the contrast adaptation properties of neurons and their location relative to pinwheels in the orientation preference map. We measured orientation preference maps in cat cortex using optical intrinsic signal imaging. We then characterized the contrast adaptation properties of single neurons located close to pinwheels, in iso‐orientation zones, and at regions in between. We found little evidence of differential contrast sensitivity of neurons adapted to zero contrast. However, after adaptation to their preferred orientation at high contrast, changes in both contrast and response gain were greater for neurons near pinwheels compared with other map regions. Therefore, in the adapted state, which is probably typical during natural viewing, there is a spatial map of contrast sensitivity that is associated with the orientation preference map. This differential adaptation revealed a new dimension of cortical functional organization, linking the contrast adaptation of cells with the orientation preference of their nearest neighbours.