Motion perception correlates with volitional but not reflexive eye movements.

Visually-driven actions and perception are traditionally ascribed to the dorsal and ventral visual streams of the cortical processing hierarchy. However, motion perception and the control of tracking eye movements both depend on sensory motion analysis by neurons in the dorsal stream, suggesting that the same sensory circuits may underlie both action and perception. Previous studies have suggested that multiple sensory modules may be responsible for the perception of low- and high-level motion, or the detection versus identification of motion direction. However, it remains unclear whether the sensory processing systems that contribute to direction perception and the control of eye movements have the same neuronal constraints. To address this, we examined inter-individual variability across 36 observers, using two tasks that simultaneously assessed the precision of eye movements and direction perception: in the smooth pursuit task, observers volitionally tracked a small moving target and reported its direction; in the ocular following task, observers reflexively tracked a large moving stimulus and reported its direction. We determined perceptual-oculomotor correlations across observers, defined as the correlation between each observer's mean perceptual precision and mean oculomotor precision. Across observers, we found that: (i) mean perceptual precision was correlated between the two tasks; (ii) mean oculomotor precision was correlated between the tasks, and (iii) oculomotor and perceptual precision were correlated for volitional smooth pursuit, but not reflexive ocular following. Collectively, these results demonstrate that sensory circuits with common neuronal constraints subserve motion perception and volitional, but not reflexive eye movements.

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.

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.

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.

Comparing acceleration and speed tuning in macaque MT: physiology and modeling.

Studies of individual neurons in area MT have traditionally investigated their sensitivity to constant speeds. We investigated acceleration sensitivity in MT neurons by comparing their responses to constant steps and linear ramps in stimulus speed. Speed ramps constituted constant accelerations and decelerations between 0 and 240 degrees /s. Our results suggest that MT neurons do not have explicit acceleration sensitivity, although speed changes affected their responses in three main ways. First, accelerations typically evoked higher responses than the corresponding deceleration rate at all rates tested. We show that this can be explained by adaptation mechanisms rather than differential processing of positive and negative speed gradients. Second, we inferred a cell's preferred speed from the responses to speed ramps by finding the stimulus speed at the latency-adjusted time when response amplitude peaked. In most cells, the preferred speeds inferred from deceleration were higher than those for accelerations of the same rate or from steps in stimulus speed. Third, neuron responses to speed ramps were not well predicted by the transient or sustained responses to steps in stimulus speed. Based on these findings, we developed a model incorporating adaptation and a neuron's speed tuning that predicted the higher inferred speeds and lower spike rates for deceleration responses compared with acceleration responses. This model did not predict acceleration-specific responses, in accordance with the lack of acceleration sensitivity in the neurons. The outputs of this single-cell model were passed to a population-vector-based model used to estimate stimulus speed and acceleration. We show that such a model can accurately estimate relative speed and acceleration using information from the population of neurons in area MT.

Rapid processing of retinal slip during saccades in macaque area MT.

The primate middle temporal area (MT) is involved in the analysis and perception of visual motion, which is generated actively by eye and body movements and passively when objects move. We studied the responses of single cells in area MT of awake macaques, comparing the direction tuning and latencies of responses evoked by wide-field texture motion during fixation (passive viewing) and during rewarded, target-directed saccades and non-rewarded, spontaneous saccades over the same stationary texture (active viewing). We found that MT neurons have similar motion sensitivity and direction-selectivity for retinal slip associated with active and passive motion. No cells showed reversals in direction tuning between the active and passive viewing conditions. However, mean latencies were significantly different for saccade-evoked responses (30 ms) and stimulus-evoked responses (67 ms). Our results demonstrate that neurons in area MT retain their direction-selectivity and display reduced processing times during saccades. This rapid, accurate processing of peri-saccadic motion may facilitate post-saccadic ocular following reflexes or corrective saccades.

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.

Torsional eye movements during psychophysical testing with rotating patterns.

Torsional eye movements were measured while subjects viewed a large, high contrast windmill pattern rotating at 53 degrees /s or a small (5 degrees diameter) dot pattern rotating at 115 degrees /s. Both stimuli generated rotational eye movements consisting of torsional optokinetic nystagmus (tOKN) superimposed on a slow torsional drift in the direction of pattern rotation. With the wide-field windmill stimulus, torsional drifts of up to 7 degrees over 20 s were found. The dot pattern produced drifts of up to 2 degrees over 5-20 s. In both cases, the slow-phase speeds during tOKN were low (0.5-1 degrees /s). We conclude that reductions in slip speed are minimal with rotating stimuli, so torsional eye speeds will have a minimal effect on investigations of rotational motion aftereffect strength and perceived speed. While the slow-phase tOKN gain is low, the slow drift in torsional eye position will have significant effects on psychophysical results when the tests rely on keeping selected regions of the stimulus confined to specific areas of the retina, as is the case for phantom or remote motion aftereffects.