Opto-locomotor reflexes of mice to reverse-phi stimuli.

In a reverse-phi stimulus, the contrast luminance of moving dots is reversed each displacement step. Under those conditions, the direction of the moving dots is perceived in the direction opposite of the displacement direction of the dots. In this study, we investigate if mice respond oppositely to phi and reverse-phi stimuli. Mice ran head-fixed on a Styrofoam ball floating on pressurized air at the center of a large dome. We projected random dot patterns that were displaced rightward or leftward, using either a phi or a reverse-phi stimulus. For phi stimuli, changes in direction caused the mice to reflexively compensate and adjust their running direction in the direction of the displaced pattern. We show that for reverse-phi stimuli mice compensate in the direction opposite to the displacement direction of the dots, in accordance with the perceived direction of displacement in humans for reverse-phi stimuli.

Transcranial Alternating Current Stimulation Attenuates Neuronal Adaptation.

We previously showed that brief application of 2 mA (peak-to-peak) transcranial currents alternating at 10 Hz significantly reduces motion adaptation in humans. This is but one of many behavioral studies showing that weak currents applied to the scalp modulate neural processing. Transcranial stimulation has been shown to improve perception, learning, and a range of clinical symptoms. Few studies, however, have measured the neural consequences of transcranial current stimulation. We capitalized on the strong link between motion perception and neural activity in the middle temporal (MT) area of the macaque monkey to study the neural mechanisms that underlie the behavioral consequences of transcranial alternating current stimulation. First, we observed that 2 mA currents generated substantial intracranial fields, which were much stronger in the stimulated hemisphere (0.12 V/m) than on the opposite side of the brain (0.03 V/m). Second, we found that brief application of transcranial alternating current stimulation at 10 Hz reduced spike-frequency adaptation of MT neurons and led to a broadband increase in the power spectrum of local field potentials. Together, these findings provide a direct demonstration that weak electric fields applied to the scalp significantly affect neural processing in the primate brain and that this includes a hitherto unknown mechanism that attenuates sensory adaptation.SIGNIFICANCE STATEMENT Transcranial stimulation has been claimed to improve perception, learning, and a range of clinical symptoms. Little is known, however, how transcranial current stimulation generates such effects, and the search for better stimulation protocols proceeds largely by trial and error. We investigated, for the first time, the neural consequences of stimulation in the monkey brain. We found that even brief application of alternating current stimulation reduced the effects of adaptation on single-neuron firing rates and local field potentials; this mechanistic insight explains previous behavioral findings and suggests a novel way to modulate neural information processing using transcranial currents. In addition, by developing an animal model to help understand transcranial stimulation, this study will aid the rational design of stimulation protocols for the treatment of mental illnesses, and the improvement of perception and learning.

Evidence and Counterevidence in Motion Perception.

Sensory neurons gather evidence in favor of the specific stimuli to which they are tuned, but they could improve their sensitivity by also taking counterevidence into account. The Bours-Lankheet model for motion detection uses counterevidence that relies on a specific combination of the ON and OFF channels in the early visual system. Specifically, the model detects pairs of flashes that occur separated in space and time. If the flashes have the same contrast polarity, they are interpreted as evidence in favor of the corresponding motion. But if they have opposite contrasts, they are interpreted as evidence against it. This mechanism provides an explanation for reverse-phi (the perceived reversal of an apparent motion stimulus due to periodic contrast-inversions) that is a conceptual departure from the standard explanations of the effect. Here, we investigate this counterevidence mechanism by measuring directional tuning curves of neurons in the primary visual and middle temporal cortex areas of awake, behaving macaques using constant-contrast and inverting-contrast moving dot stimuli. Our electrophysiological data support the Bours-Lankheet model and suggest that the counterevidence computation occurs at an early stage of neural processing not captured by the standard models.

Similar adaptation effects in primary visual cortex and area MT of the macaque monkey under matched stimulus conditions.

Recent stimulus history, or adaptation, can alter neuronal response properties. Adaptation effects have been characterized in a number of visually responsive structures, from the retina to higher visual cortex. However, it remains unclear whether adaptation effects across stages of the visual system take a similar form in response to a particular sensory event. This is because studies typically probe a single structure or cortical area, using a stimulus ensemble chosen to provide potent drive to the cells of interest. Here we adopt an alternative approach and compare adaptation effects in primary visual cortex (V1) and area MT using identical stimulus ensembles. Previous work has suggested these areas adjust to recent stimulus drive in distinct ways. We show that this is not the case: adaptation effects in V1 and MT can involve weak or strong loss of responsivity and shifts in neuronal preference toward or away from the adapter, depending on stimulus size and adaptation duration. For a particular stimulus size and adaptation duration, however, effects are similar in nature and magnitude in V1 and MT. We also show that adaptation effects in MT of awake animals depend strongly on stimulus size. Our results suggest that the strategies for adjusting to recent stimulus history depend more strongly on adaptation duration and stimulus size than on the cortical area. Moreover, they indicate that different levels of the visual system adapt similarly to recent sensory experience.

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.

Temporal integration of focus position signal during compensation for pursuit in optic flow.

Observer translation results in optic flow that specifies heading. Concurrent smooth pursuit causes distortion of the retinal flow pattern for which the visual system compensates. The distortion and its perceptual compensation are usually modeled in terms of instantaneous velocities. However, apart from adding a velocity to the flow field, pursuit also incrementally changes the direction of gaze. The effect of gaze displacement on optic flow perception has received little attention. Here we separated the effects of velocity and gaze displacement by measuring the perceived two-dimensional focus position of rotating flow patterns during pursuit. Such stimuli are useful in the current context because the two effects work in orthogonal directions. As expected, the instantaneous pursuit velocity shifted the perceived focus orthogonally to the pursuit direction. Additionally, the focus was mislocalized in the direction of the pursuit. Experiments that manipulated the presentation duration, flow speed, and uncertainty of the focus location supported the idea that the latter component of mislocalization resulted from temporal integration of the retinal trajectory of the focus. Finally, a comparison of the shift magnitudes obtained in conditions with and without pursuit (but with similar retinal stimulation) suggested that the compensation for both effects uses extraretinal information.

The role of motion capture in an illusory transformation of optic flow fields.

In the optic flow illusion, the focus of an expanding optic flow field appears shifted when uniform flow is transparently superimposed. The shift is in the direction of the uniform flow, or "inducer." Current explanations relate the transformation of the expanding optic flow field to perceptual subtraction of the inducer signal. Alternatively, the shift might result from motion capture acting on the perceived focus position. To test this alternative, we replaced expanding target flow with contracting or rotating flow. Current explanations predict focus shifts in expanding and contracting flows that are opposite but of equal magnitude and parallel to the inducer. In rotary flow, the current explanations predict shifts that are perpendicular to the inducer. In contrast, we report larger shift for expansion than for contraction and a component of shift parallel to the inducer for rotary flow. The magnitude of this novel component of shift depended on the target flow speed, the inducer flow speed, and the presentation duration. These results support the idea that motion capture contributes substantially to the optic flow illusion.

An illusory transformation of optic flow fields without local motion interactions.

The focus of expansion (FOE) of a radially expanding optic flow pattern that is overlapped by unidirectional laminar flow is perceptually displaced in the direction of that laminar flow. There is continuing debate on whether this effect is due to local or global motion interactions. Here, we show psychophysically that under conditions without local motion transparency the illusion becomes weaker but can still be observed. In our experiments, the radial and laminar-flow fields were not presented with overlap but separately to the left and right halves of the visual field with a blank vertical strip of 15 degrees horizontal width in between. The illusory shift observed in this condition cannot be explained by local motion interactions because (a) no transparent motion was present in the stimulus, and (b) the receptive fields of cortical cells involved in the analysis of local motion cross the vertical midline of the visual field to a limited extent. We conclude that global motion detectors that integrate motion from both halves of the visual field play a role in shifting the perceived position of the FOE and that local motion interactions may be sufficient, but are not necessary for the optic flow illusion to occur.

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.

The effect of dendritic topology on firing patterns in model neurons.

Neuronal firing patterns are influenced by both membrane properties and dendritic morphology. Distinguishing two sources of morphological variability-metrics and topology-we investigate the extent to which model neurons that have the same metrical and membrane properties can still produce different firing patterns as a result of differences in dendritic topology. Within a set of dendritic trees that have the same number of terminal segments and the same total dendritic length, we show that firing frequency strongly correlates with topology as expressed by the mean dendritic path length. The effect of dendritic topology on firing frequency is bigger for trees with equal segment diameters than for trees whose segment diameters obey Rall's 3/2 power law. If active dendritic channels are present, dendritic topology influences not only firing frequency but also type of firing (regular, bursting).