Robert H. Wurtz

NEURONAL MECHANISMS OF VISUAL STABILITY

Human vision is stable and continuous in spite of the incessant interruptions produced by saccadic eye movements. These rapid eye movements serve vision by directing the high resolution fovea rapidly from one part of the visual scene to another. They should detract from vision because they generate two major problems: displacement of the retinal image with each saccade and blurring of the image during the saccade. This review considers the substantial advances in understanding the neuronal mechanisms underlying this visual stability derived primarily from neuronal recording and inactivation studies in the monkey, an excellent model for systems in the human brain. For the first problem, saccadic displacement, two neuronal candidates are salient. First are the neurons in frontal and parietal cortex with shifting receptive fields that provide anticipatory activity with each saccade and are driven by a corollary discharge. These could provide the mechanism for a retinotopic hypothesis of visual stability and possibly for a transsaccadic memory hypothesis, The second neuronal mechanism is provided by neurons whose visual response is modulated by eye position (gain field neurons) or are largely independent of eye position (real position neurons), and these neurons could provide the basis for a spatiotopic hypothesis. For the second problem, saccadic suppression, visual masking and corollary discharge are well established mechanisms, and possible neuronal correlates have been identified for each.

Influence of the thalamus on spatial visual processing in frontal cortex

Each of our movements activates our own sensory receptors, and therefore keeping track of self-movement is a necessary part of analysing sensory input. One way in which the brain keeps track of self-movement is by monitoring an internal copy, or corollary discharge, of motor commands. This concept could explain why we perceive a stable visual world despite our frequent quick, or saccadic, eye movements: corollary discharge about each saccade would permit the visual system to ignore saccade-induced visual changes. The critical missing link has been the connection between corollary discharge and visual processing. Here we show that such a link is formed by a corollary discharge from the thalamus that targets the frontal cortex. In the thalamus, neurons in the mediodorsal nucleus relay a corollary discharge of saccades from the midbrain superior colliculus to the cortical frontal eye field. In the frontal eye field, neurons use corollary discharge to shift their visual receptive fields spatially before saccades. We tested the hypothesis that these two components—a pathway for corollary discharge and neurons with shifting receptive fields—form a circuit in which the corollary discharge drives the shift. First we showed that the known spatial and temporal properties of the corollary discharge predict the dynamic changes in spatial visual processing of cortical neurons when saccades are made. Then we moved from this correlation to causation by isolating single cortical neurons and showing that their spatial visual processing is impaired when corollary discharge from the thalamus is interrupted. Thus the visual processing of frontal neurons is spatiotemporally matched with, and functionally dependent on, corollary discharge input from the thalamus. These experiments establish the first link between corollary discharge and visual processing, delineate a brain circuit that is well suited for mediating visual stability, and provide a framework for studying corollary discharge in other sensory systems.

Guarding the gateway to cortex with attention in visual thalamus

The massive visual input from the eye to the brain requires selective processing of some visual information at the expense of other information, a process referred to as visual attention. Increases in the responses of visual neurons with attention have been extensively studied along the visual processing streams in monkey cerebral cortex, from primary visual areas to parietal and frontal cortex. Here we show, by recording neurons in attending macaque monkeys (Macaca mulatta), that attention modulates visual signals before they even reach cortex by increasing responses of both magnocellular and parvocellular neurons in the first relay between retina and cortex, the lateral geniculate nucleus (LGN). At the same time, attention decreases neuronal responses in the adjacent thalamic reticular nucleus (TRN). Crick argued for such modulation of the LGN by observing that it is inhibited by the TRN, and suggested that “if the thalamus is the gateway to the cortex, the reticular complex might be described as the guardian of the gateway”, a reciprocal relationship we now show to be more than just hypothesis. The reciprocal modulation in LGN and TRN appears only during the initial visual response, but the modulation of LGN reappears later in the response, suggesting separate early and late sources of attentional modulation in LGN.

Modulation of neuronal activity by target uncertainty

Visual scenes are composed of many elements and although we can appreciate a scene as a whole, we can only move our eyes to one element of the scene at a time. As visual scenes become more complex, the number of potential targets in the scene increases, and the uncertainty that any particular one will be selected for an eye movement also increases. How motor systems accommodate this target uncertainty remains unknown. The activities of neurons in both the cerebral cortex and superior colliculus are modulated by this selection process. We reasoned that activity associated with target uncertainty should be evident in the saccadic motor system at the final stages of neural processing, in the superior colliculus. By systematically changing the number of stimuli from which a selection must be made and recording from superior colliculus neurons, we found that as the target uncertainty increased, the neural activity preceding target selection decreased. These results indicate that neurons within the final common pathway for movement generation are active well in advance of the selection of a particular movement. This early activity varies with the probability that a particular movement will be selected.

A grid system and a microsyringe for single cell recording

The designs of two instruments are presented which have proven to be useful in single cell and chemical injection studies performed in awake monkeys. The first is a plastic grid that acts as a guide to produce parallel penetrations with either a microelectrode or microsyringe. The second is a syringe for injecting microliter quantities of a solution that also allows recording of neuronal activity.

Brain Circuits for the Internal Monitoring of Movements

Each movement we make activates our own sensory receptors, thus causing a problem for the brain: the spurious, movement-related sensations must be discriminated from the sensory inputs that really matter, those representing our environment. Here we consider circuits for solving this problem in the primate brain. Such circuits convey a copy of each motor command, known as a corollary discharge (CD), to brain regions that use sensory input. In the visual system, CD signals may help to produce a stable visual percept from the jumpy images resulting from our rapid eye movements. A candidate pathway for providing CD for vision ascends from the superior colliculus to the frontal cortex in the primate brain. This circuit conveys warning signals about impending eye movements that are used for planning subsequent movements and analyzing the visual world. Identifying this circuit has provided a model for studying CD in other primate sensory systems and may lead to a better understanding of motor and mental disorders.

Saccadic omission: why we do not see a grey-out during a saccadic eye movement.

Abstract We investigated why we have no perception of a smeared image resulting from the reduction in contrast (grey-out) occurring at the retina during saccadic eye movements. By turning on light in the experimental room only during the eye movement, we were able to show that this grey-out was perceived as a smeared image of the visual scene. However, when the experimental room was illuminated before and/or after the saccade as well as during the saccade, perception of the grey-out was obliterated. During a period of fixation, perception of a blank image comparable in duration to an eye movement could also be eliminated by a preceding or following clear image. We conclude that lack of perception during saccadic eye movements made in normal contoured environments results primarily from the visual “masking” effect of a clear image before and/or after the eye movement acting on the grey-out during the eye movement. This “saccadic omission” is entirely a visual phenomenon and is far more powerful than the usually studied elevation of visual threshold for detection of a flash, “saccadic suppression.”

Subcortical Modulation of Attention Counters Change Blindness

Change blindness is the failure to see large changes in a visual scene that occur simultaneously with a global visual transient. Such visual transients might be brief blanks between visual scenes or the blurs caused by rapid or saccadic eye movements between successive fixations. Shifting attention to the site of the change counters this “blindness” by improving change detection and reaction time. We developed a change blindness paradigm for visual motion and then showed that presenting an attentional cue diminished the blindness in both humans and old world monkeys. We then replaced the visual cue with weak electrical stimulation of an area in the monkeys brainstem, the superior colliculus, to see if activation at such a late stage in the eye movement control system contributes to the attentional shift that counters change blindness. With this stimulation, monkeys more easily detected changes and had shorter reaction times, both characteristics of a shift of attention.

Superior Colliculus Cell Responses Related to Eye Movements in Awake Monkeys

Single cell responses were recorded from the superior colliculus of awake monkeys trained to move their eyes. A class of cells that discharged before eye movements was found in the intermediate and deep layers of the colliculus. The response of the cells was most vigorous before saccadic eye movements within a particular range of directions. These cells had no visual receptive fields, and visually guided eye movements were not necessary for their discharge, since they responded in total darkness before spontaneous eye movements and vestibular nystagmus.

Attentional modulation of thalamic reticular neurons.

The major pathway for visual information reaching cerebral cortex is through the lateral geniculate nucleus (LGN) of the thalamus. Acting on this vital relay is another thalamic nucleus, the thalamic reticular nucleus (TRN). This nucleus receives topographically organized collaterals from both thalamus and cortex and sends similarly organized projections back to thalamus. The inputs to the TRN are excitatory, but the output back to the thalamic relay is inhibitory, providing an ideal organization for modulating visual activity during early processing. This functional architecture led Crick in 1984 to hypothesize that TRN serves to direct a searchlight of attention to different regions of the topographic map; however, despite the substantial influence of this hypothesis, the activity of TRN neurons has never been determined during an attention task. We have determined the nature of the response of visual TRN neurons in awake monkeys, and the modulation of that response as the monkeys shifted attention between visual and auditory stimuli. Visual TRN neurons had a strong (194 spikes/s) and fast (25 ms latency) transient increase of activity to spots of light falling in their receptive fields, as well as high background firing rate (45 spikes/s). When attention shifted to the spots of light, the amplitude of the transient visual response typically increased, whereas other neuronal response characteristics remained unchanged. Thus, as predicted previously, TRN activity is modified by shifts of visual attention, and these attentional changes could influence visual processing in LGN via the inhibitory connections back to the thalamus.