Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT.

Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal adaptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-induced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation.

Implied motion activation in cortical area MT can be explained by visual low-level features.

To investigate form-related activity in motion-sensitive cortical areas, we recorded cell responses to animate implied motion in macaque middle temporal (MT) and medial superior temporal (MST) cortex and investigated these areas using fMRI in humans. In the single-cell studies, we compared responses with static images of human or monkey figures walking or running left or right with responses to the same human and monkey figures standing or sitting still. We also investigated whether the view of the animate figure (facing left or right) that elicited the highest response was correlated with the preferred direction for moving random dot patterns. First, figures were presented inside the cell's receptive field. Subsequently, figures were presented at the fovea while a dynamic noise pattern was presented at the cell's receptive field location. The results show that MT neurons did not discriminate between figures on the basis of the implied motion content. Instead, response preferences for implied motion correlated with preferences for low-level visual features such as orientation and size. No correlation was found between the preferred view of figures implying motion and the preferred direction for moving random dot patterns. Similar findings were obtained in a smaller population of MST cortical neurons. Testing human MT+ responses with fMRI further corroborated the notion that low-level stimulus features might explain implied motion activation in human MT+. Together, these results suggest that prior human imaging studies demonstrating animate implied motion processing in area MT+ can be best explained by sensitivity for low-level features rather than sensitivity for the motion implied by animate figures.

Directional anisotropy of motion responses in retinotopic cortex.

Recently, evidence has emerged for a radial orientation bias in early visual cortex. These results predict that in early visual cortex a tangential bias should be present for motion direction. We tested this prediction in a human imaging study, using a translating random dot pattern that slowly rotated its motion direction 360 degrees in cycles of 54 s. In addition, polar angle and eccentricity mapping were performed. This allowed the measurement of the BOLD response across the visual representations of the different retinotopic areas. We found that, in V1, V2, and V3, BOLD responses were consistently enhanced for centrifugal and centripetal motion, relative to tangential motion. The relative magnitude of the centrifugal and centripetal response biases changed with visual eccentricity. We found no motion direction biases in MT+. These results are in line with previously observed anisotropies in motion sensitivity across the visual field. However, the observation of radial motion biases in early visual cortex is surprising considering the evidence for a radial orientation bias. An additional experiment was performed to resolve this apparent conflict in results. The additional experiment revealed that the observed motion direction biases most likely originate from anisotropies in long range horizontal connections within visual cortex.

Temporal Limits of Visual Motion Processing: Psychophysics and Neurophysiology.

Under optimal conditions, just 3-6 ms of visual stimulation suffices for humans to see motion. Motion perception on this timescale implies that the visual system under these conditions reliably encodes, transmits, and processes neural signals with near-millisecond precision. Motivated by in vitro evidence for high temporal precision of motion signals in the primate retina, we investigated how neuronal and perceptual limits of motion encoding relate. Specifically, we examined the correspondence between the time scale at which cat retinal ganglion cells in vivo represent motion information and temporal thresholds for human motion discrimination. The timescale for motion encoding by ganglion cells ranged from 4.6 to 91 ms, and depended non-linearly on temporal frequency, but not on contrast. Human psychophysics revealed that minimal stimulus durations required for perceiving motion direction were similarly brief, 5.6-65 ms, and similarly depended on temporal frequency but, above ~10%, not on contrast. Notably, physiological and psychophysical measurements corresponded closely throughout (r = 0.99), despite more than a 20-fold variation in both human thresholds and optimal timescales for motion encoding in the retina. The match in absolute values of the neurophysiological and psychophysical data may be taken to indicate that from the lateral geniculate nucleus (LGN) through to the level of perception little temporal precision is lost. However, we also show that integrating responses from multiple neurons can improve temporal resolution, and this potential trade-off between spatial and temporal resolution would allow for loss of temporal resolution after the LGN. While the extent of neuronal integration cannot be determined from either our human psychophysical or neurophysiological experiments and its contribution to the measured temporal resolution is unknown, our results demonstrate a striking similarity in stimulus dependence between the temporal fidelity established in the retina and the temporal limits of human motion discrimination.

Tuning for temporal interval in human apparent motion detection.

Detection of apparent motion in random dot patterns requires correlation across time and space. It has been difficult to study the temporal requirements for the correlation step because motion detection also depends on temporal filtering preceding correlation and on integration at the next levels. To specifically study tuning for temporal interval in the correlation step, we performed an experiment in which prefiltering and postintegration were held constant and in which we used a motion stimulus containing coherent motion for a single interval value only. The stimulus consisted of a sparse random dot pattern in which each dot was presented in two frames only, separated by a specified interval. On each frame, half of the dots were refreshed and the other half was a displaced reincarnation of the pattern generated one or several frames earlier. Motion energy statistics in such a stimulus do not vary from frame to frame, and the directional bias in spatiotemporal correlations is similar for different interval settings. We measured coherence thresholds for left-right direction discrimination by varying motion coherence levels in a Quest staircase procedure, as a function of both step size and interval. Results show that highest sensitivity was found for an interval of 17-42 ms, irrespective of viewing distance. The falloff at longer intervals was much sharper than previously described. Tuning for temporal interval was largely, but not completely, independent of step size. The optimal temporal interval slightly decreased with increasing step size. Similarly, the optimal step size decreased with increasing temporal interval.

The parallel between reverse-phi and motion aftereffects.

Periodically flipping the contrast of a moving pattern causes a reversal of the perceived direction of motion. This direction reversal, known as reverse-phi motion, has been generally explained with the notion that flipping contrasts actually shifted the balance of motion energy toward the opposite direction. In this sense, the reversal is trivial because any suitable motion energy detector would be optimally excited in a direction opposite to that for regular motion. This notion, however, does not address the question how these two types of motion are initially detected. Here we show several perceptual phenomena indicating that low-level detection of the two types of motion is quite different. Reverse-phi motion percepts in many respects behave more like motion aftereffects than like regular motion. Motion adaptation causes reduced activity during a stationary test stimulus, which by means of directional opponency leads to motion perceived in the opposite direction. Our findings suggest that reverse-phi motion similarly reduces the activity of low-level motion detectors.

Unraveling adaptation and mutual inhibition in perceptual rivalry.

When the visual system is confronted with incompatible images in the same part of the visual field, the conscious percept switches back and forth between the rivaling stimuli. Such spontaneous flips provide important clues to the neuronal basis for visual awareness. The general idea is that two representations compete for dominance in a process of mutual inhibition, in which adaptation shifts the balance to and fro. The inherent nonlinear nature of the rivalrous flip-flop and its stochastic behavior, however, made it impossible to disentangle inhibition and adaptation. Here we report a general method to measure the time course, and asymmetries, of mechanisms involved in perceptual rivalry. Supported by model simulations, we show the dynamics of opponent interactions between mutual inhibition and adaptation. The findings not only provide new insight into the mechanism underlying rivalry but also offer new opportunities to study and compare a wide range of bistable processes in the brain and their relation to visual awareness.

Spatio-temporal requirements for direction selectivity in area 18 and PMLS complex cells.

The spatio-temporal requirements for direction selectivity were studied in two extrastriate motion processing areas in the cat, area 18 and the posteromedial lateral suprasylvian cortex (PMLS). Direction, velocity and pixel size of random pixel arrays (RPA) were adjusted for each neuron and direction selectivity was measured as a function of step size and delay for a given optimal velocity. A subset of direction selective complex cells in area 18 was tuned to intermediate step size and delay combinations rather than the smoothest motion (band-pass cells). Other area 18 complex cells responded best to the smallest value of step size and delay (low-pass cells). Tuning varied with the pixel size of the RPA. Cells with tuning for smaller pixels favoured a preference for non-smooth motion. Area 18 cells with lower spatial resolution showed larger optimal and maximal step sizes. For a subset of the cells in area 18, we measured direction selectivity for extensive step-delay combinations, covering multiple velocities. Results showed that most cells were tuned to narrow range of step-delay combinations, and that the optimal step size was independent of temporal delay. Direction selective complex cells in PMLS were tuned to larger pixel sizes than those in area 18, although the distributions did overlap. In contrast to area 18, PMLS cells preferred the smoothest motion, irrespective of RPA pixel size.

The motion reverse correlation (MRC) method: a linear systems approach in the motion domain.

We introduce the motion reverse correlation method (MRC), a novel stimulus paradigm based on a random sequence of motion impulses. The method is tailored to investigate the spatio-temporal dynamics of motion selectivity in cells responding to moving random dot patterns. Effectiveness of the MRC method is illustrated with results obtained from recordings in both anesthetized cats and an awake, fixating macaque monkey. Motion tuning functions are computed by reverse correlating the response of single cells with a rapid sequence of displacements of a random pixel array (RPA). Significant correlations between the cell's responses and various aspects of stimulus motion are obtained at high temporal resolution. These correlations provide a detailed description of the temporal dynamics of, for example, direction tuning and velocity tuning. In addition, with a spatial array of independently moving RPAs, the MRC method can be used to measure spatial as well as temporal receptive field properties. We demonstrate that MRC serves as a powerful and time-efficient tool for quantifying receptive field properties of motion selective cells that yields temporal information that cannot be derived from existing methods.

Binocular correlation does not improve coherence detection for fronto-parallel motion.

We studied the low-level interactions between motion coherence detection and binocular correlation detection. It is well-established that e.g. depth information from motion parallax and from binocular disparities is effectively integrated. The question we aimed to answer is whether such interactions also exist at the very first correlation level that both mechanisms might have in common. First we quantitatively compared motion coherence detection and binocular correlation detection using similar stimuli (random pixels arrays, RPAs) and the same noise masking paradigm (luminance signal to noise ratio, LSNR). This showed that human observers are much more sensitive to motion than to binocular correlation. Adding noise therefore has a much stronger effect on binocular correlation than on motion detection. Next we manipulated the shape of the stimulus aperture to equalize LSNR thresholds for motion and binocular correlation. Motion sensitivity could be progressively reduced by shortening the length of the motion path, while keeping the aperture area constant. Changing the shape of the aperture did not affect binocular correlation sensitivity. A 'balanced' stimulus, one with equal strengths of motion and binocular correlation signals was then used to study the mutual interactions. In accordance with previous results, motion was found to greatly facilitate binocular correlation. Binocular correlation, however did not facilitate motion detection. We conclude that interactions are asymmetrical; fronto-parallel motion is primarily detected monocularly and this information can then be used to facilitate binocular correlation, but binocular correlation cannot improve motion sensitivity.

Speed and direction response profiles of neurons in macaque MT and MST show modest constraint line tuning.

Several models of heading detection during smooth pursuit rely on the assumption of local constraint line tuning to exist in large scale motion detection templates. A motion detector that exhibits pure constraint line tuning responds maximally to any 2D-velocity in the set of vectors that can be decomposed into the central, or classic, preferred velocity (the shortest vector that still yields the maximum response) and any vector orthogonal to that. To test this assumption, we measured the firing rates of isolated middle temporal (MT) and medial superior temporal (MST) neurons to random dot stimuli moving in a range of directions and speeds. We found that as a function of 2D velocity, the pooled responses were best fit with a 2D Gaussian profile with a factor of elongation, orthogonal to the central preferred velocity, of roughly 1.5 for MST and 1.7 for MT. This means that MT and MST cells are more sharply tuned for speed than they are for direction; and that they indeed show some level of constraint line tuning. However, we argue that the observed elongation is insufficient to achieve behavioral heading discrimination accuracy on the order of 1-2 degrees as reported before.

Spike-interval triggered averaging reveals a quasi-periodic spiking alternative for stochastic resonance in catfish electroreceptors.

Catfish detect and identify invisible prey by sensing their ultra-weak electric fields with electroreceptors. Any neuron that deals with small-amplitude input has to overcome sensitivity limitations arising from inherent threshold non-linearities in spike-generation mechanisms. Many sensory cells solve this issue with stochastic resonance, in which a moderate amount of intrinsic noise causes irregular spontaneous spiking activity with a probability that is modulated by the input signal. Here we show that catfish electroreceptors have adopted a fundamentally different strategy. Using a reverse correlation technique in which we take spike interval durations into account, we show that the electroreceptors generate a supra-threshold bias current that results in quasi-periodically produced spikes. In this regime stimuli modulate the interval between successive spikes rather than the instantaneous probability for a spike. This alternative for stochastic resonance combines threshold-free sensitivity for weak stimuli with similar sensitivity for excitations and inhibitions based on single interspike intervals.

Temporal interactions in direction-selective complex cells of area 18 and the posteromedial lateral suprasylvian cortex (PMLS) of the cat.

Temporal interactions in direction-sensitive complex cells in area 18 and the posteromedial lateral suprasylvian cortex (PMLS) were studied using a reverse correlation method. Reverse correlograms to combinations of two temporally separated motion directions were examined and compared in the two areas. A comparison to the first-order reverse correlograms allowed us to identify nonlinear suppression or facilitation due to pairwise combinations of motion directions. Results for area 18 and PMLS were very different. Area 18 showed a single type of nonlinear behavior: similar directions facilitated and opposite directions suppressed spike probability. This effect was most pronounced for motion steps that followed each other immediately and decreased with increasing delay between steps. In PMLS, the picture was much more diverse. Some cells exhibited nonlinear interactions, that were opposite to those in area 18 (facilitation for opposite directions and suppression for similar ones), while the majority did not show a systematic interaction profile. We conclude that nonlinear second-order reverse correlation characteristics reveal different functional properties, despite similarities in the first-order reverse correlation profiles. Directional interactions in time revealed optimal integration of similar directions in area 18, but motion opponency--at least in some cells--in PMLS.

Dynamics of directional selectivity in MT receptive field centre and surround.

We studied receptive field organization of motion-sensitive neurons in macaque middle temporal cortical area (MT), by mapping direction selectivity in space and in time. Stimuli consisted of pseudorandom sequences of single motion steps presented simultaneously at many different receptive field locations. Spatio-temporal receptive field profiles were constructed by cross-correlating stimuli and spikes. The resulting spike-triggered averages revealed centre-surround organization. The temporal dynamics of the receptive fields were generally biphasic with increased probability for the preferred direction at short latency (50-70 ms) and decreased probability at longer latency (80-100 ms). The response latency of the receptive field surround was on average 16 ms longer than that of the centre. Our results show that surround input and biphasic behaviour reflect two different mechanisms, which make MT cells specifically sensitive to motion contrast in space and time.

Temporal dynamics of direction tuning in motion-sensitive macaque area MT.

We studied the temporal dynamics of motion direction sensitivity in macaque area MT using a motion reverse correlation paradigm. Stimuli consisted of a random sequence of motion steps in eight different directions. Cross-correlating the stimulus with the resulting neural activity reveals the temporal dynamics of direction selectivity. The temporal dynamics of direction selectivity at the preferred speed showed two phases along the time axis: one phase corresponding to an increase in probability for the preferred direction at short latencies and a second phase corresponding to a decrease in probability for the preferred direction at longer latencies. The strength of this biphasic behavior varied between neurons from weak to very strong and was uniformly distributed. Strong biphasic behavior suggests optimal responses for motion steps in the antipreferred direction followed by a motion step in the preferred direction. Correlating spikes to combinations of motion directions corroborates this distinction. The optimal combination for weakly biphasic cells consists of successive steps in the preferred direction, whereas for strongly biphasic cells, it is a reversal of directions. Comparing reverse correlograms to combinations of stimuli to predictions based on correlograms for individual directions revealed several nonlinear effects. Correlations for successive presentations of preferred directions were smaller than predicted, which could be explained by a static nonlinearity (saturation). Correlations to pairs of (nearly) opposite directions were larger than predicted. These results show that MT neurons are generally more responsive when sudden changes in motion directions occur, irrespective of the preferred direction of the neurons. The latter nonlinearities cannot be explained by a simple static nonlinearity at the output of the neuron, but most likely reflect network interactions.

Dynamics of directional selectivity in area 18 and PMLS of the cat.

Visual latencies and temporal dynamics of area 18 and PMLS direction-selective complex cells were defined with a reverse correlation method. The method allowed us to analyze the time course of responses to motion steps, without confounding temporal integration effects. Several measures of response latency and direction tuning dynamics were quantified: optimal latency (OL), latency of first and last significant responses (FSR, LSR), the increase and decrease of direction sensitivity in time, and the change of direction tuning in time. FSR, OL and LSR values for PMLS and area 18 largely overlapped. The small differences in mean latencies (3-4 ms for FSR and OL and 11.9 ms for the LSR) were not statistically significant. All cells in area 18 and the vast majority of cells in PMLS showed no systematic changes in preferred direction (monophasic neurons). In PMLS 5 out of 41 cells showed a reversal of preferred direction after approximately 56 ms relative to their OL (biphasic neurons). Monophasic cells showed no systematic changes in direction tuning width during the interval from FSR to LSR. In both areas, development of direction sensitivity was significantly faster than return to the non-direction sensitive state, but no significant difference was found between the two areas. We conclude that, for the monophasic type of direction-selective complex cells, the dynamics of primary motion processing are highly comparable for area 18 and PMLS. This suggests that motion information is predominantly processed in parallel, presumably based on input from the fast conducting thalamocortical Y-pathway.

Velocity dependence of the interocular transfer of dynamic motion aftereffects.

It is well established that motion aftereffects (MAEs) can show interocular transfer (IOT); that is, motion adaptation in one eye can give a MAE in the other eye. Different quantification methods and different test stimuli have been shown to give different IOT magnitudes, varying from no to almost full IOT. In this study, we examine to what extent IOT of the dynamic MAE (dMAE), that is the MAE seen with a dynamic noise test pattern, varies with velocity of the adaptation stimulus. We measured strength of dMAE by a nulling method. The aftereffect induced by adaptation to a moving random-pixel array was compensated (nulled), during a brief dynamic test period, by the same kind of motion stimulus of variable luminance signal-to-noise ratio (LSNR). The LSNR nulling value was determined in a Quest-staircase procedure. We found that velocity has a strong effect on the magnitude of IOT for the dMAE. For increasing speeds from 1.5 deg s(-1) to 24 deg s(-1) average IOT values increased about linearly from 18% to 63% or from 32% to 83%, depending on IOT definition. The finding that dMAEs transfer to an increasing extent as speed increases, suggests that binocular cells play a more dominant role at higher speeds.

On the velocity tuning of area 18 complex cell responses to moving textures.

Unlike simple cells, complex cells of area 18 give a directionally selective response to motion of random textures, indicating that they may play a special role in motion detection. We therefore investigated how texture motion, and especially its velocity, is represented by area 18 complex cells. Do these cells have separable spatial and temporal tunings or are these nonseparable? To answer this question, we measured responses to moving random pixel arrays as a function of both pixel size and velocity, for a set of 63 directionally selective complex cells. Complex cells generally responded to a fairly wide range of pixel sizes and velocities. Variations in pixel size of the random pixel array only caused minor changes in the cells' preferred velocity. For nearly all cells the data much better fitted a model in which pixel size and velocity act separately, than a model in which pixel size and velocity interact so as to keep temporal-frequency sensitivity constant. Our conclusion is that the studied population of special complex cells in area 18 are true motion detectors, rather than temporal-frequency tuned neurons.