Peter H. Schiller

State dependent activity in monkey visual cortex

SummaryThis study examined the extent to which the responses of single cells in the striate cortex (V1) and the extrastriate cortex (V4) of the alert rhesus monkey are modulated by visual stimuli whose relevance in a behavioral task is varied. The animal had to detect the repetition of a visual pattern (i.e. detect similarity), preceded by a randomized number of alternations between two different patterns. The responses produced by the last, reward contingent stimulus were compared with responses obtained to that same stimulus earlier in the sequence. Modulatory effects in V1 were moderate: 31% of the cells (63 of 200) showed response increments of 20% or more to the last, reward contingent stimulus. In V4 the effects were much more pronounced: 72% of the cells (110 of 154) showed modulatory effects of more than 20%. In V4 but not in V1 orientation tuning curves showed a significant narrowing as well as a peak response increment to the behaviorally salient stimulus, suggesting a feature specific mechanism associated with the detection of similarity. Although a response decrement was observed in many cells during the repeated alternations, this effect was significantly smaller than the modulation produced by the detection of similarity. Controls included the presentation of novel stimuli during the presentation sequence which did not produce an enhanced response. It is hypothesized that the feature specific effects reported here are produced by higher order feedback systems.

Role of the color-opponent and broad-band channels in vision.

The functions of the primate color-opponent and broad-band channels were assessed by examining the visual capacities of rhesus monkeys following selective lesions of parvocellular and magnocellular lateral geniculate nucleus, which respectively relay these two channels to the cortex. Parvocellular lesions impaired color vision, high spatial-frequency form vision, and fine stereopsis. Magnocellular lesions impaired high temporal-frequency flicker and motion perception but produced no deficits in stereopsis. Low spatial-frequency form vision, stereopsis, and brightness perception were unaffected by either lesion. Much as the rods and cones of the retina can be thought of as extending the range of vision in the intensity domain, we propose that the color-opponent channel extends visual capacities in the wavelength and spatial-frequency domains whereas the broad-band channel extends them in the temporal domain.

The ON and OFF channels of the visual system

In the vertebrate retina, all photoreceptors hyperpolarize in response to light. In the outer retina, at the bipolar cell level, a dual system is created from the cones forming the ON and OFF channels. In the rod system a similar arrangement is found, but the ON and OFF channels in many species are formed using an amacrine cell network in the inner retina. Physiological experiments in which the ON bipolar cells are pharmacologically blocked reveal that in the primate the two channels remain largely segregated in the geniculostriate system until they reach the cortex, where they converge upon single cells. Behavioral studies show that following ON channel block, notable deficits arise in the detection of light increments but not light decrements. These and related studies suggest that the ON and OFF channels optimize information transfer to the CNS by providing excitatory signals for both increases and decreases in light energy.

The Color-Opponent and Broad-Band Channels of the Primate Visual System

Physiological, anatomical and psychophysical studies have identified several parallel channels of information processing in the primate visual system. Two of these, the color-opponent and the broad-band channels, originate in the retina and remain in part segregated through several higher cortical stations. To improve understanding of their function, recent studies have examined the visual capacities of monkeys following selective disruption of these channels. Color vision, fine- but not coarse-form vision and stereopsis are severely impaired in the absence of the color-opponent channel, whereas motion and flicker perception are impaired at high but not low temporal frequencies in the absence of the broad-band channel. The results suggest that the color-opponent channel extends the range of vision in the spatial and wavelength domains, and that the broad-band channel extends it in the temporal domain. Lesion studies also indicate that these channels must reach higher cortical centers through extrastriate regions other than just area V4 and the middle temporal area, and that the analysis performed by these two regions cannot be uniquely identified with specific visual capacities.

Eye fields in the frontal lobes of primates.

Two eye fields have been identified in the frontal lobes of primates: one is situated dorsomedially within the frontal cortex and will be referred to as the eye field within the dorsomedial frontal cortex (DMFC); the other resides dorsolaterally within the frontal cortex and is commonly referred to as the frontal eye field (FEF). This review documents the similarities and differences between these eye fields. Although the DMFC and FEF are both active during the execution of saccadic and smooth pursuit eye movements, the FEF is more dedicated to these functions. Lesions of DMFC minimally affect the production of most types of saccadic eye movements and have no effect on the execution of smooth pursuit eye movements. In contrast, lesions of the FEF produce deficits in generating saccades to briefly presented targets, in the production of saccades to two or more sequentially presented targets, in the selection of simultaneously presented targets, and in the execution of smooth pursuit eye movements. For the most part, these deficits are prevalent in both monkeys and humans. Single-unit recording experiments have shown that the DMFC contains neurons that mediate both limb and eye movements, whereas the FEF seems to be involved in the execution of eye movements only. Imaging experiments conducted on humans have corroborated these findings. A feature that distinguishes the DMFC from the FEF is that the DMFC contains a somatotopic map with eyes represented rostrally and hindlimbs represented caudally; the FEF has no such topography. Furthermore, experiments have revealed that the DMFC tends to contain a craniotopic (i.e., head-centered) code for the execution of saccadic eye movements, whereas the FEF contains a retinotopic (i.e., eye-centered) code for the elicitation of saccades. Imaging and unit recording data suggest that the DMFC is more involved in the learning of new tasks than is the FEF. Also with continued training on behavioural tasks the responsivity of the DMFC tends to drop. Accordingly, the DMFC is more involved in learning operations whereas the FEF is more specialized for the execution of saccadic and smooth pursuit eye movements.

Eye Movements Modulate Visual Receptive Fields of V4 Neurons

The receptive field, defined as the spatiotemporal selectivity of neurons to sensory stimuli, is central to our understanding of the neuronal mechanisms of perception. However, despite the fact that eye movements are critical during normal vision, the influence of eye movements on the structure of receptive fields has never been characterized. Here, we map the receptive fields of macaque area V4 neurons during saccadic eye movements and find that receptive fields are remarkably dynamic. Specifically, before the initiation of a saccadic eye movement, receptive fields shrink and shift towards the saccade target. These spatiotemporal dynamics may enhance information processing of relevant stimuli during the scanning of a visual scene, thereby assisting the selection of saccade targets and accelerating the analysis of the visual scene during free viewing.

Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey

SummaryRecent work has shown that humans and monkeys utilize both retinal error and eye position signals to compute the direction and amplitude of saccadic eye movements (Hallett and Lightstone 1976a, b; Mays and Sparks 1980b). The aim of this study was to examine the role the frontal eye fields (FEF) and the superior colliculi (SC) play in this computation. Rhesus monkeys were trained to acquire small, briefly flashed spots of light with saccadic eye movements. During the latency period between target extinction and saccade initiation, their eyes were displaced, in total darkness, by electrical stimulation of either the FEF, the SC or the abducens nucleus area. Under such conditions animals compensated for the electrically induced ocular displacement and correctly reached the visual target area, suggesting that both a retinal error and eye position error signal were computed. The amplitude and direction of the electrically induced saccades depended not only on the site stimulated but also on the amplitude and direction of the eye movement initiated by the animal to acquire the target. When the eye movements initiated by the animal coincided with the saccades initiated by electrical stimulation, the resultant saccade was the weighted average of the two, where one weighting factor was the intensity of the electrical stimulus. Animals did not acquire targets correctly when their eyes were displaced, prior to their intended eye movements, by stimulating in the abducens nucleus area. After bilateral ablation of either the FEF or the SC monkeys were still able to acquire visual targets when their eyes were displaced, prior to saccade initiation, by electrical stimulation of the remaining intact structure. These results suggest that neither the FEF nor the SC is uniquely responsible for the combined computation of the retinal error and the eye position error signals.

Spatial frequency and orientation tuning dynamics in area V1

Spatial frequency (SF) and orientation tuning are intrinsic properties of neurons in primary visual cortex (area V1). To investigate the neural mechanisms mediating selectivity in the awake animal, we measured the temporal dynamics of SF and orientation tuning. We adapted a high-speed reverse-correlation method previously used to characterize orientation tuning dynamics in anesthetized animals to estimate efficiently the complete spatiotemporal receptive fields in area V1 of behaving macaques. We found that SF and orientation tuning are largely separable over time in single neurons. However, spatiotemporal receptive fields also contain a small nonseparable component that reflects a significant difference in response latency for low and high SF stimuli. The observed relationship between stimulus SF and latency represents a dynamic shift in SF tuning, and suggests that single V1 neurons might receive convergent input from the magno- and parvocellular processing streams. Although previous studies with anesthetized animals suggested that orientation tuning could change dramatically over time, we find no substantial evidence of dynamic changes in orientation tuning.

The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey

The effects of V4, MT, and combined V4 + MT lesions were assessed on a broad range of visual capacities that included measures of contrast sensitivity, wavelength and brightness discrimination, form vision, pattern vision, motion and flicker perception, stereopsis, and the selection of stimuli that were less prominent than those with which they appeared in stimulus arrays. The major deficit observed was a loss in the ability, after V4 lesions, to select such less prominent stimuli; this was the case irrespective of the manner in which the stimulus arrays were made visible, using either luminance, chrominance, motion, or stereoscopic depth as surface media. In addition, V4 lesions yielded mild deficits in color, brightness, and form vision whereas MT lesions yielded mild to moderate deficits in motion and flicker perception. Both lesions produced mild deficits in contrast sensitivity, shape-from-motion perception, and yielded increased reaction times on many of the tasks. The impairment resulting from combined V4 and MT lesions was not greater than the sum of the deficits of either lesion. None of the lesions produced significant deficits in stereopsis. The findings suggest that (1) area V4 is part of a neural system that is involved in extracting stimuli from the visual scene that elicit less neural activity early in the visual system than do other stimuli with which they appear and (2) several other extrastriate regions and more than just two major cortical processing streams contribute to the processing of basic visual functions in the extrastriate cortex.

Single unit activity in the frontal eye fields of unanesthetized monkeys during eye and head movement.

SummarySingle unit activity in the frontal eye field was investigated in unanesthetized monkeys during eye and head movement. Two types of cells (I and II) were found. Type I fired during voluntary saccadic movement occuring in a given direction and also during the fast phase of optokinetic and vestibular nystagmus. Cells of this type were silent during smooth pursuit movement and the slow phase of nystagmus. It was found that the firing pattern of Type I cells was maintained irrespective of head movement.Type II cells fired during smooth pursuit eye movements and the slow phase of nystagmus; these units displayed a steady discharge when the eyes were oriented in a specific position. Also this type of cell maintained its characteristic discharge during head movement. A separate population of frontal eye field cells was found to be exclusively related to head turning.