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The response of a sensory neuron to an unchanging stimulus typically adapts, showing decreases in response gain that are accompanied by changes in the shape of tuning curves. It remains unclear whether these changes arise purely due to spike rate adaptation within single neurons or whether they are dependent on network interactions between neurons. Further, it is unclear how the timescales of neural and perceptual adaptation are related. To examine this issue, we compared speed tuning of middle temporal (MT) and medial superior temporal neurons in macaque visual cortex after adaptation to two different reference speeds. For 75% of speed-tuned units, adaptation caused significant changes in tuning that could be explained equally well as lateral shifts, vertical gain changes, or both. These tuning changes occurred rapidly, as both neuronal firing rate and Fano factor showed no evidence of changing beyond the first 500 ms after motion onset, and the magnitude of tuning curve changes showed no difference between trials with adaptation durations shorter or longer than 1 s. Importantly, the magnitude of tuning shifts was correlated with the transient-sustained index, which measures a well characterized form of rapid response adaptation in MT, and is likely associated with changes at the level of neuronal networks. Tuning curves changed in a manner that increased neuronal sensitivity around the adapting speed, consistent with improvements in human and macaque psychophysical performance that we observed over the first several hundred ms of adaptation.

The primate visual cortex exhibits a remarkable degree of interconnectivity. Each visual area receives an average of 10 to 15 inputs, many of them from cortical areas with overlapping, but not identical, functional properties. In this study, we assessed the functional significance of this anatomical parallelism to the middle temporal area (MT) of the macaque visual cortex. MT receives major feedforward inputs from areas V1, V2, and V3, but little is known about the properties of each of these pathways. We previously demonstrated that reversible inactivation of V2 and V3 causes a disproportionate degradation of tuning for binocular disparity of MT neurons, relative to direction tuning (Ponce et al., 2008). Here we show that MT neurons continued to encode speed and size information during V2/3 inactivation; however, many became significantly less responsive to fast speeds and others showed a modest decrease in surround suppression. These changes resemble previously reported effects of reducing stimulus contrast (Pack et al., 2005; Krekelberg et al., 2006), but we show here that they differ in their temporal dynamics. We find no evidence that the indirect pathways selectively target different functional regions within MT. Overall, our findings suggest that the indirect pathways to MT primarily convey modality-specific information on binocular disparity, but that they also contribute to the processing of stimuli moving at fast speeds.

Surround suppression contributes to important functions in visual processing, such as figure-ground segregation; however, this benefit comes at the cost of decreased neuronal sensitivity. Studies of receptive fields at several levels of the visual hierarchy have demonstrated that surround suppression is reduced for low contrast stimuli, thereby improving neuronal sensitivity. We investigated whether this reduction of surround suppression reflects a general processing strategy to boost sensitivity for weak signals by summing them over a larger region of the visual field (spatial integration) or if the reduction is limited to specialized stimulus conditions. To do this, we used stochastic motion stimuli to measure surround suppression in area MT of alert macaque monkeys. While varying stimulus size we also varied the strength of two other critical stimulus features: contrast and coherence (i.e., the proportion of dots moving in the preferred direction of the neuron). We found that reducing stimulus contrast weakened surround suppression, but reducing stimulus coherence had the opposite effect, indicating that diminished surround suppression is not a universal response to stimuli of low signal-to-noise. This can be partially explained by our other finding, which is that surrounds in MT are very broadly direction tuned. Instead of producing a reduction of surround suppression that would improve the ability of the neuron to integrate preferred direction motion, low coherence stimuli activated the broadly tuned surrounds relatively better than the centers, which are generally more direction selective. Our results are consistent with a normalization mechanism of surround suppression that pools broadly across multiple stimulus dimensions.

The contribution of sensory neurons to perceptual decisions about external stimulus events has received much attention, but it is less clear how sensory responses are integrated over time to produce decisions that are both rapid and reliable. To address this issue, we recorded from middle temporal area and medial superior temporal area neurons in rhesus macaques performing a task requiring the detection and discrimination of unpredictable speed changes. We examined how neuronal activity encoded the sign of the speed change and predicted the animals' behavioral judgments and reaction times, with a focus on the timescales over which neuronal activity is informative. False detection trials, on which animals reported a speed change even though none had occurred, were grouped according to the animals' discrimination judgment. By comparing the neuronal responses between the two groups of false detection trials, we were able to predict the animals' choices from the sensory activity of single neurons at levels significantly better than chance. These choice probability measurements were strongest using spike counts in an 80 ms window ending 150 ms before a choice saccade began, but significant choice probabilities were observed in windows as short as 10 ms. While the maximum deviation in spiking rate following a speed change is evident in the transient response, averaging neuronal activity in longer time windows can be more informative about both the stimulus and the animals' behavioral judgments. Thus the timescales found in this study represent a trade-off between producing rapid reactions and overcoming the noise inherent in short time windows.

The primate visual system is arranged hierarchically, starting from the retina and continuing through a series of extrastriate visual areas. Selectivity for motion is first found in individual neurons in the primate visual cortex (V1), in which many simple cells respond selectively to the direction and speed of moving stimuli. Beyond simple cells, most studies of direction selectivity have focused on either V1 complex cells or neurons in the middle temporal area (MT/V5). To understand how visual information is transferred along this pathway, we have studied all three types of neurons, using a reverse correlation procedure to obtain high spatial and temporal resolution maps of activity for different motion stimuli. Most complex and MT cells showed strong second-order interactions, indicating that they were tuned for particular displacements of an apparent motion stimulus. The spatiotemporal structure of these interactions showed a high degree of similarity between the populations of V1 complex cells and MT cells, in terms of the spatiotemporal limits and preferences for motion and their two-dimensional spatial structure. Much of the structure in the V1 and MT second-order kernels could be accounted for on the basis of the first-order responses of V1 simple cells, under the assumption of a Reichardt or motion-energy type of computation.

The integration of visual information is a critical task that is performed by neurons in the extrastriate cortex of the primate brain. For motion signals, integration is complicated by the geometry of the visual world, which renders some velocity measurements ambiguous and others incorrect. The ambiguity arises because neurons in the early stages of visual processing have small receptive fields, which can only recover the component of motion perpendicular to the orientation of a contour (the aperture problem). Unambiguous motion signals are located at end points and corners, which are referred to as terminators. However, when an object moves behind an occluding surface, motion measurements made at the terminators formed by the intersection of the object and the occluder are generally not consistent with the direction of object motion. To study how cortical neurons integrate these different motion cues, we used variations on the classic “barber pole” stimulus and measured the responses of neurons in the middle temporal area (MT or V5) of extrastriate cortex of alert macaque monkeys. Our results show that MT neurons are more strongly influenced by the unambiguous motion signals generated by terminators than to the ambiguous signals generated by contours. Furthermore, these neurons respond better to terminators that are intrinsic to a moving object than to those that are accidents of occlusion. V1 neurons show similar response patterns to local cues (contours and terminators), but for large stimuli, they do not reflect the global motion direction computed by MT neurons. These observations are consistent with psychophysical findings that show that our perception of moving objects often depends on the motion of terminators.

The middle temporal visual area (MT) of the owl monkey is anatomically organized with respect to both preferred direction of motion and different types of center–surround interaction. The latter organization consists of clusters of neurons whose receptive fields have antagonistic surrounds that render them unresponsive to wide-field motion (local motion columns) interdigitated with groups of neurons whose receptive fields have additive surrounds and thus respond best to wide-field motion (wide-field motion columns).To learn whether the information in these regions remained segregated further along the visual pathways, we made injections of retrograde tracers into two visual areas to which MT projects [the medial superior temporal area (MST) and fundus of the superior temporal sulcus (FST)] and then labeled the wide-field and local organization using 2-deoxyglucose. In complementary experiments, we injected anterograde tracers into regions of MT that we had mapped using microelectrode recordings.Injections into both dorsal FST and ventral MST labeled clusters of cell bodies in MT that were concentrated within wide-field motion columns, whereas injections into dorsal MST labeled neurons predominantly within local motion columns. Results from the anterograde tracer experiments corroborated these findings. The high degree of specificity in the connections reinforces a model of functional organization for wide-field versus local motion processing within MT. Our data support the previously reported division of FST into separate dorsal and ventral areas, and they also suggest that MST of the owl monkey is, like MST of the macaque, functionally organized with respect to local versus wide-field motion processing.

To generate behavioral responses based on sensory input, motor areas of the brain must interpret, or “read out,” signals from sensory maps. Our experiments tested several algorithms for how the motor systems for smooth pursuit and saccadic eye movements might extract a usable signal of target velocity from the distributed representation of velocity in the middle temporal visual area (MT or V5). Using microstimulation, we attempted to manipulate the velocity information within MT while monkeys tracked a moving visual stimulus. We examined the effects of the microstimulation on smooth pursuit and on the compensation for target velocity shown by saccadic eye movements. Microstimulation could alter both the speed and direction of the motion estimates of both types of eye movements and could also cause monkeys to generate pursuit even when the visual target was actually stationary. The pattern of alterations suggests that microstimulation can introduce an additional velocity signal into MT and that the pursuit and saccadic systems usually compute a vector average of the visually evoked and microstimulation-induced velocity signals (pursuit, 55 of 122 experiments; saccades, 70 of 122). Microstimulation effects in a few experiments were consistent with vector summation of these two signals (pursuit, 6 of 122; saccades, 2 of 122). In the remainder of the experiments, microstimulation caused either an apparent impairment in motion processing (pursuit, 47 of 122; saccades, 41 of 122) or had no effect (pursuit, 14 of 122; saccades, 9 of 122). Within individual experiments, the effects on pursuit and saccades were usually similar, but the occasional striking exception suggests that the two eye movement systems may perform motion computations somewhat independently.

Using noninvasive functional magnetic resonance imaging (fMRI) technique, we analyzed the responses in human area MT with regard to visual motion, color, and luminance contrast sensitivity, and retinotopy. As in previous PET studies, we found that area MT responded selectively to moving (compared to stationary) stimuli. The location of human MT in the present fMRI results is consistent with that of MT in earlier PET and anatomical studies. In addition we found that area MT has a much higher contrast sensitivity than that in several other areas, including primary visual cortex (V1). Functional MRI half- amplitudes in V1 and MT occurred at approximately 15% and 1% luminance contrast, respectively. High sensitivity to contrast and motion in MT have been closely associated with magnocellular stream specialization in nonhuman primates. Human psychophysics indicates that visual motion appears to diminish when moving color-varying stimuli are equated in luminance. Electrophysiological results from macaque MT suggest that the human percept could be due to decreases in firing of area MT cells at equiluminance. We show here that fMRI activity in human MT does in fact decrease at and near individually measured equiluminance. Tests with visuotopically restricted stimuli in each hemifield produced spatial variations in fMRI activity consistent with retinotopy in human homologs of macaque areas V1, V2, V3, and VP. Such activity in area MT appeared much less retinotopic, as in macaque. However, it was possible to measure the interhemispheric spread of fMRI activity in human MT (half amplitude activation across the vertical meridian = approximately 15 degrees).