Mingsha Zhang

Saccadic Dysmetria and Adaptation after Lesions of the Cerebellar Cortex

We studied the effects of small lesions of the oculomotor vermis of the cerebellar cortex on the ability of monkeys to execute and adapt saccadic eye movements. For saccades in one horizontal direction, the lesions led to an initial gross hypometria and a permanent abolition of the capacity for rapid adaptation. Mean saccade amplitude recovered from the initial hypometria, although variability remained high. A series of hundreds of repetitive saccades in the same direction resulted in gradual decrement of amplitude. Saccades in other directions were less strongly affected by the lesions. We suggest the following. (1) The cerebellar cortex is constantly recalibrating the saccadic system, thus compensating for rapid biomechanical changes such as might be caused by muscle fatigue. (2) A mechanism capable of slow recovery from dysmetria is revealed despite the permanent absence of rapid adaptation.

The proprioceptive representation of eye position in monkey primary somatosensory cortex

The cerebral cortex must have access to an eye position signal, as humans can report passive changes in eye position in total darkness, and visual responses in many cortical areas are modulated by eye position. The source of this signal is unknown. Here we demonstrate a representation of eye position in monkey primary somatosensory cortex, in the representation of the trigeminal nerve, near cells with a tactile representation of the contralateral brow. The neurons have eye position signals that increase monotonically with increasing orbital eccentricity from near the center of gaze, with directionally selectivity tuned in a Gaussian manner. All directions of eye position are represented in a single hemisphere. The signal is proprioceptive, because it can be obliterated by anesthetizing the contralateral orbit. It is not related to foveal or peripheral visual stimulation, and it represents the position of the eye in the head and not the angle of gaze in space.

Psychophysical Evidence for Spatiotopic Processing in Area MT in a Short-Term Memory for Motion Task

The middle temporal (MT) area has long been established as a cortical area involved in the encoding of motion information and has been thought to do so in retinotopic coordinates. It was previously shown that memory for motion has a spatial component by demonstrating that subjects do significantly worse on a match-to-sample task when the stimuli to be compared were spatially separated. The distance at which performance deteriorated (the critical spatial separation) increased at increasing eccentricities, suggesting that area MT was involved in the process. In this study, we asked whether optimal performance occurred when the stimuli were in the same retinotopic or spatiotopic coordinates. We found that the performance was best when the stimuli appeared in the same location in space rather than the same retinal location, after an eye movement. We also found that the relationship between retinal eccentricity and the critical spatial separation approximated that of area MT, as found previously. We conclude that area MT plays an important role in the memory for motion process and that this is carried out in spatiotopic coordinates. This conclusion supports the hypothesis that MT processing may have a spatiotopic component.

Shifted encoding strategy in retinal luminance adaptation: from firing rate to neural correlation

Neuronal responses to prolonged stimulation attenuate over time. Here, we ask a fundamental question: is adaptation a simple process for the neural system during which sustained input is ignored, or is it actually part of a strategy for the neural system to adjust its encoding properties dynamically? After simultaneously recording the activities of a group of bullfrogs retinal ganglion cells (dimming detectors) in response to sustained dimming stimulation, we applied a combination of information analysis approaches to explore the time-dependent nature of information encoding during the adaptation. We found that at the early stage of the adaptation, the stimulus information was mainly encoded in firing rates, whereas at the late stage of the adaptation, it was more encoded in neural correlations. Such a transition in encoding properties is not a simple consequence of the attenuation of neuronal firing rates, but rather involves an active change in the neural correlation strengths, suggesting that it is a strategy adopted by the neural system for functional purposes. Our results reveal that in encoding a prolonged stimulation, the neural system may utilize concerted, but less active, firings of neurons to encode information.

Perisaccadic Receptive Field Expansion in the Lateral Intraparietal Area

Humans and monkeys have access to an accurate representation of visual space despite a constantly moving eye. One mechanism by which the brain accomplishes this is by remapping visual receptive fields around the time of a saccade. In this process a neuron can be excited by a probe stimulus in the current receptive field, and also simultaneously by a probe stimulus in the location that will be brought into the neurons receptive field by the saccade (the future receptive field), even before saccade begins. Here we show that perisaccadic neuronal excitability is not limited to the current and future receptive fields but encompasses the entire region of visual space across which the current receptive field will be swept by the saccade. A computational model shows that this receptive field expansion is consistent with the propagation of a wave of activity across the cerebral cortex as saccade planning and remapping proceed.

Asymmetric Influence of Egocentric Representation onto Allocentric Perception

Objects in the visual world can be represented in both egocentric and allocentric coordinates. Previous studies have found that allocentric representation can affect the accuracy of spatial judgment relative to an egocentric frame, but not vice versa. Here we asked whether egocentric representation influenced the processing speed of allocentric perception. We measured the manual reaction time of human subjects in a position discrimination task in which the behavioral response purely relied on the targets allocentric location, independent of its egocentric position. We used two conditions of stimulus location: the compatible condition—allocentric left and egocentric left or allocentric right and egocentric right; the incompatible condition—allocentric left and egocentric right or allocentric right and egocentric left. We found that egocentric representation markedly influenced allocentric perception in three ways. First, in a given egocentric location, allocentric perception was significantly faster in the compatible condition than in the incompatible condition. Second, as the target became more eccentric in the visual field, the speed of allocentric perception gradually slowed down in the incompatible condition but remained unchanged in the compatible condition. Third, egocentric-allocentric incompatibility slowed allocentric perception more in the left egocentric side than the right egocentric side. These results cannot be explained by interhemispheric visuomotor transformation and stimulus-response compatibility theory. Our findings indicate that each hemisphere preferentially processes and integrates the contralateral egocentric and allocentric spatial information, and the right hemisphere receives more ipsilateral egocentric inputs than left hemisphere does.

A spatially nonselective baseline signal in parietal cortex reflects the probability of a monkey’s success on the current trial

Significance Cortical neurons are often active when they are not participating in sensorimotor processes. Here we show that this baseline activity reflects a modulatory signal predicting the monkey’s success on a difficult task without specifying what the monkey perceives or will do. The activity correlates inversely with the monkey’s recent history of success, so that a period of failure is associated with an increase in the baseline and predicts an increase in the monkey’s likelihood of success. The activity is not related to the spatial locus of the monkey’s visual attention. We suggest that this activity is the cortical manifestation of an arousal or state process that controls the efficiency of an animal’s behavior without specifying the nature of that behavior. We recorded the activity of neurons in the lateral intraparietal area of two monkeys while they performed two similar visual search tasks, one difficult, one easy. Each task began with a period of fixation followed by an array consisting of a single capital T and a number of lowercase t’s. The monkey had to find the capital T and report its orientation, upright or inverted, with a hand movement. In the easy task the monkey could explore the array with saccades. In the difficult task the monkey had to continue fixating and find the capital T in the visual periphery. The baseline activity measured during the fixation period, at a time in which the monkey could not know if the impending task would be difficult or easy or where the target would appear, predicted the monkey’s probability of success or failure on the task. The baseline activity correlated inversely with the monkeys recent history of success and directly with the intensity of the response to the search array on the current trial. The baseline activity was unrelated to the monkey’s spatial locus of attention as determined by the location of the cue in a cued visual reaction time task. We suggest that rather than merely reflecting the noise in the system, the baseline signal reflects the cortical manifestation of modulatory state, motivational, or arousal pathways, which determine the efficiency of cortical sensorimotor processing and the quality of the monkey’s performance.

Parietal Cortical Neuronal Activity Is Selective for Express Saccades

Saccadic eye movements are central to primate behavior and serve to move the eyes to visual objects of interest. Express saccades, unlike regular saccades, occur with very short reaction times, a behavior necessary for speeded reactions in goal-directed behavior. Previous studies have shown that introduction of a blank interval (gap) between the fixation point offset and the saccadic target onset leads to an increase in the number of express saccades and that the superior colliculus plays a crucial role in the generation of express saccades. A longstanding hypothesis asserted that express saccades are mediated largely by a subcortical circuit, circumventing extrastriate visual cortex. An alternative “posterior pathway” hypothesis proposed the involvement of posterior parietal cortex. In the present study, using a gap saccade task, we investigated the role of nonhuman primates lateral intraparietal cortex (LIP) in generation of express saccades. We show that roughly half of recorded LIP neurons were modulated during the gap interval. Moreover, a group of neurons with persistent activity in a memory-guided saccade task enhanced their activity during express saccades relative to that during regular saccades. After reducing the targets certainty by increasing the potential target locations, neuronal activity remained in the similar level during express saccades but markedly reduced during regular saccades that correlated with the increase of saccadic reaction time in the regular saccade. Our results suggest that area LIP is directly involved in generating saccades in express mode.

Covert attention regulates saccadic reaction time by routing between different visual-oculomotor pathways

Covert attention modulates saccadic performance, e.g., the abrupt onset of a task-irrelevant visual stimulus grabs attention as measured by a decrease in saccadic reaction time (SRT). The attentional advantage bestowed by the task-irrelevant stimulus is short-lived: SRT is actually longer ~200 ms after the onset of a stimulus than it is when no stimulus appears, known as inhibition of return. The mechanism by which attention modulates saccadic reaction is not well-understood. Here, we propose two possible mechanisms: by selective routing of the visuomotor signal through different pathways (routing hypothesis) or by general modulation of the speed of visuomotor transformation (shifting hypothesis). To test them, we designed a cue gap paradigm in which a 100-ms gap was introduced between the fixation point disappearance and the target appearance to the conventional cued visual reaction time paradigm. The cue manipulated the location of covert attention, and the gap interval resulted in a bimodal distribution of SRT, with an early mode (express saccade) and a late mode (regular saccade). The routing hypothesis predicts changes in the proportion of express saccades vs. regular saccades, whereas the shifting hypothesis predicts a shift of SRT distribution. The addition of the cue had no effect on mean reaction time of express and regular saccades, but it changed the relative proportion of two modes. These results demonstrate that the covert attention modification of the mean SRT is largely attributed to selective routing between visuomotor pathways rather than general modulation of the speed of visuomotor transformation.

Firing Frequency Maxima of Fast-Spiking Neurons in Human, Monkey, and Mouse Neocortex

Cortical fast-spiking (FS) neurons generate high-frequency action potentials (APs) without apparent frequency accommodation, thus providing fast and precise inhibition. However, the maximal firing frequency that they can reach, particularly in primate neocortex, remains unclear. Here, by recording in human, monkey, and mouse neocortical slices, we revealed that FS neurons in human association cortices (mostly temporal) could generate APs at a maximal mean frequency (Fmean) of 338 Hz and a maximal instantaneous frequency (Finst) of 453 Hz, and they increase with age. The maximal firing frequency of FS neurons in the association cortices (frontal and temporal) of monkey was even higher (Fmean 450 Hz, Finst 611 Hz), whereas in the association cortex (entorhinal) of mouse it was much lower (Fmean 215 Hz, Finst 342 Hz). Moreover, FS neurons in mouse primary visual cortex (V1) could fire at higher frequencies (Fmean 415 Hz, Finst 582 Hz) than those in association cortex. We further validated our in vitro data by examining spikes of putative FS neurons in behaving monkey and mouse. Together, our results demonstrate that the maximal firing frequency of FS neurons varies between species and cortical areas.