Jacob Duijnhouwer

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.

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.

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.

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.

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.

tACS- What goes on inside? The neural consequences of transcranial alternating current stimulation

There is considerable evidence for clinical and behavioral efficacy of transcranial alternating current stimulation (tACS). The effects range from suppressing Parkinsonian tremors to augmenting human learning and memory. Despite widespread use, the neurobiological mechanism of actions of tACS on the brain is unclear. We have taken a threefold approach to probe tACS mechanisms. First, we examined the behavioral effects of tACS on human motion perception. Second, we used known motion models to generate predictions about neural mechanisms that could produce the effects. Third, we tested these predictions by directly measuring tACS-induced neural activity changes in the macaque brain.

Transcranial electrical stimulation affects adaptation of MT/V5 neurons in awake behaving macaques

Despite widespread use in clinical and behavioral studies, the mechanisms of action of transcranial electrical stimulation (tES) are poorly understood. We partially attribute this to the lack of in-vivo animal models and have started to probe the influence of tES on the wellexplored macaque visual system, specifically area MT. Previously we have shown that tES reduces the motion aftereffect in human subjects. This leads to the hypothesis that neurons adapt less during tES.

The opto-locomotor reflex as a tool to measure sensitivity to moving random dot patterns in mice

We designed a method to quantify mice visual function by measuring reflexive opto-locomotor responses. Mice were placed on a Styrofoam ball at the center of a large dome on the inside of which we projected moving random dot patterns. Because we fixed the heads of the mice in space and the ball was floating on pressurized air, locomotion of the mice was translated to rotation of the ball, which we registered. Sudden onsets of rightward or leftward moving patterns caused the mice to reflexively change their running direction. We quantified the opto-locomotor responses to different pattern speeds, luminance contrasts, and dot sizes. We show that the method is fast and reliable and the magnitude of the reflex is stable within sessions. We conclude that this opto-locomotor reflex method is suitable to quantify visual function in mice.