Dark-habituation increases the dark-background-contingent upshift of gaze in macaque monkeys.

What is the effect of prior experience on sensorimotor behavior? We studied the following intriguing behavior: monkeys fixating a small target direct their gaze above the target if the background is dark. Fixating a target once on a bright background, then on a dark background, yields 2 gaze directions, typically one above the other; hence the name, 'dark-background-contingent upshift of gaze', which is abbreviated as 'upshift'. Is the upshift only an attempt to avoid using the fovea in the dark? If it is, we might expect to also observe a downshift and a sideshift. We studied gaze direction in a large group of 10 rhesus monkeys from Tübingen, to which we added published data from 4 cynomolgus monkeys from Rehovot. The upshift was ubiquitous, and there was no systematic sideshift. What is the function of the upshift? Is it related to vision in the dark? Here, we concentrate on the effect of the monkeys' previous training. Seven of the 14 monkeys were accustomed to working in the dark ('dark-habituated'), while the other 7 had worked in bright ambient light ('bright-habituated'). The main result of this study is that the dark-habituated monkeys had a much larger upshift: the mean upshift was 2.2° in the dark-habituated monkeys, versus 0.5° in the bright-habituated. Thus, the upshift depends on habituation; the size of the upshift reflects months-long cumulative experience. These findings suggest that the function of the upshift is indeed related to seeing in the dark.

Persistence of the dark-background-contingent gaze upshift during visual fixations of rhesus monkeys.

During visual fixations, the eyes are directed so that the image of the target (object of interest) falls on the fovea. An exception to this rule was described in macaque monkeys (though not in humans): dark background induces a gaze shift upwards, sometimes large enough to shift the target's image off the fovea. In this article we address an aspect not previously rigorously studied, the time course of the upshift. The time course is critical for determining whether the upshift is indeed an attribute of visual fixation or, alternatively, of saccades that precede the fixation. These alternatives lead to contrasting predictions regarding the time course of the upshift (durable if the upshift is an attribute of fixation, transient if caused by saccades). We studied visual fixations with dark and bright background in three monkeys. We confined ourselves to a single upshift-inducing session in each monkey so as not to study changes in the upshift caused by training. Already at their first sessions, all monkeys showed clear upshift. During the first 0.5 s after the eye reached the vicinity of the target, the upshift was on average larger, but also more variable, than later in the trial; this initial high value 1) strongly depended on target location and was maximal at locations high on the screen, and 2) appears to reflect mostly the intervals between the primary and correction saccades. Subsequently, the upshift stabilized and remained constant, well above zero, throughout the 2-s fixation interval. Thus there is a persistent background-contingent upshift genuinely of visual fixation.

Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease.

The term short-term saccadic adaptation (STSA) captures our ability to unconsciously move the endpoint of a saccade to the final position of a visual target that has jumped to a new location during the saccade. STSA depends on the integrity of the cerebellar vermis. We tested the hypothesis that STSA reflects the working of a cerebellar mechanism needed to avoid 'fatigue', a gradual drop in saccade amplitude during a long series of stereotypic saccades. To this end we compared the kinematics of saccades of 14 patients suffering from different forms of cerebellar disease with those of controls in two tests of STSA and a test of saccadic resilience. Controls showed an increase in saccade amplitude (SA) for outward adaptation, prompted by outward target shifts, due to an increase in saccade duration (SD) in the face of constant peak velocity (PV). The decrease in SA due to inward adaptation was, contrariwise, accompanied by a drop in PV and SD. Whereas patients with intact vermis did not differ from controls, those with vermal pathology lacked outward adaptation: SD remained constant, as did SA and PV. In contrast, vermal patients demonstrated a significant decrease in SA, paralleled by a decrease in PV but mostly unaltered SD in the inward adaptation experiment as well as in the resilience test. These findings support the notion that inward adaptation is at least partially based on uncompensated fatigue. On the other hand, outward adaptation reflects an active mechanism for the compensation of fatigue, residing in the cerebellum.

Switching of sensorimotor transformations: antisaccades and parietal cortex.

The sensorimotor processing necessary in complex realistic situations goes beyond straight-forward application of a given sensorimotor transformation. Contextual information may make it necessary to switch to another sensorimotor transformation. We studied the issue of switching by using the mixed memory prosaccade/antisaccade task. Neurons of the lateral intra-parietal area (LIP) might be involved in computing the sensorimotor transformations for both prosaccades and antisaccades. LIP neurons may also be involved in switching to the antisaccade sensorimotor transformation, when an antisaccade is requested. Some neurons in LIP show a paradoxical pattern of activity-motor in space but visual in time. Funahashi, Chafee and Goldman-Rakic reported in 1993 a complimentary pattern of activity in prefrontal cortex-visual in space but motor in time. These odd observations are explained by the hypothesis that (1) the parietal cortex contains a sensorimotor transformation module, and prefrontal cortex a context categorization module, and (2) following target onset, information flows from early visual system to parietal cortex and on to prefrontal cortex; then, a second wave of activation, contingent on a switching signal, arrives back at parietal cortex. The duration of this loop is less than 100 ms. Thus, the paradoxical activities are intermediate representations derived in the cognitive processing involved in switching sensorimotor transformations.

Single-neuron evidence for a contribution of the dorsal pontine nuclei to both types of target-directed eye movements, saccades and smooth-pursuit.

The primate dorsolateral pontine nucleus (DLPN) is a key link in a cerebro-cerebellar pathway for smooth pursuit eye movements, a pathway assumed to be anatomically segregated from tegmental circuits subserving saccades. However, the existence of afferents from several cerebrocortical and subcortical centres for saccades suggests that the DLPN and neighbouring parts of the dorsal pontine nuclei (DPN) might contribute to saccades as well. In order to test this hypothesis, we recorded from the DPN of two monkeys trained to perform smooth pursuit eye movements as well as visually and memory-guided saccades. Out of 281 neurons isolated from the DPN, 138 were responsive in oculomotor tasks. Forty-five were exclusively activated in saccade paradigms, 68 exclusively by smooth pursuit and 25 neurons showed responses in both. Pursuit-related responses reflected sensitivity to eye position, velocity or combinations of velocity and position with minor contributions of acceleration in many cases. When tested in the memory-guided saccades paradigm, 65 out of 70 neurons activated in saccade paradigms showed significant saccade-related bursts and 20 significant activity in the memory period. Our finding of saccade-related activity in the DPN in conjunction with the existence of strong anatomical input from saccade-related cerebrocortical areas suggests that the DPN serves as a precerebellar relay for both pursuit and saccade-related information originating from cerebral cortex, in addition to the classical tecto-tegmental circuitry for saccades.

Persistent LIP activity in memory antisaccades: working memory for a sensorimotor transformation.

The lateral intraparietal area (LIP) contains neurons that are active during the memory interval of memory saccades. We call these "persistent neurons." Here we study the activity of the persistent neurons in memory antisaccades, "motor" (the saccade is made toward the response field, although the response field is not stimulated visually) and "visual" (the response field is stimulated visually, but the movement is away from the field). Most persistent neurons are active during parts of the memory intervals of both visual and motor memory-antisaccades. Typically, these parts significantly overlap each other and together span the entire memory interval. The amplitude of the activity changes systematically during the memory intervals of visual and motor memory antisaccades. These changes are reflected in an antisaccade differential activity, which turns first to the visual direction and then crosses over to the motor direction. Some persistent neurons appear to show the paradoxical activity previously characterized in visual neurons; paradoxical activity accelerates the transition of the neuron's activity from visual to motor. These observations suggest that the persistent neurons reflect working memory for the computation of the antisaccade sensorimotor transformation. Ensembles of persistent neurons with different response fields may make up modules of working memory.

Paradoxical activities: insight into the relationship of parietal and prefrontal cortices.

What are the functions of the parietal and prefrontal cortices and how do these regions interact to achieve their objectives? How does context change plans for action? Are 'visual' and 'motor' well-defined attributes of neuronal activity in the association cortex? Recent studies of the saccadic system in monkeys have revealed two sets of paradoxical data: in parietal cortex, activity has visual timing but motor direction; in prefrontal cortex, activity has motor timing but visual direction. Analyzing the prefrontal and parietal data together leads to surprising insights. It appears that these paradoxical activities are intermediates in a parietal-prefrontal-parietal loop that has a rapid turnaround, and that a possibly prefrontal context-contingent signal switches sensorimotor transformations in parietal cortex.