Anna E. Ipata

Activity in the Lateral Intraparietal Area Predicts the Goal and Latency of Saccades in a Free-Viewing Visual Search Task

The purpose of saccadic eye movements is to facilitate vision, by placing the fovea on interesting objects in the environment. Eye movements are not made for reward, and they are rarely restricted. Despite this, most of our knowledge about the neural genesis of eye movements comes from experiments in which specific eye movements are rewarded or restricted. Such experiments have demonstrated that activity in the lateral intraparietal (LIP) area of the monkey correlates with the monkeys planning of a memory-guided saccade or deciding where, on the basis of motion information, to make a saccade. However, other experiments have shown that neural activity in LIP can easily be dissociated from the generation of saccadic eye movements, especially when sophisticated behavioral paradigms dissociate the monkeys locus of attention from the goal of an intended saccade. In this study, we trained monkeys to report the results of a visual search task by making a nontargeting hand movement. Once the task began, the monkeys were entirely free to move their eyes, and rewards were not contingent on the monkeys making specific eye movements. We found that neural activity in LIP predicted not only the goal of the monkeys saccades but also their saccadic latencies.

Neural Enhancement and Pre-Emptive Perception: The Genesis of Attention and the Attentional Maintenance of the Cortical Salience Map

One of the stable hypotheses in systems neuroscience is the relationship between attention and the enhancement of visual responses when an animal attends to the stimulus in its receptive field (Goldberg and Wurtz, 1972 Journal of Neurophysiology 35 560 – 574). This was first discovered in the superior colliculus of the monkey: neurons in the superficial layers of the superior colliculus responded more intensely to the onset of a stimulus during blocks of trials in which the monkey had to make a saccade to it than they did during blocks of trials in which the monkey had to continue fixating a central point and not respond to the stimulus. This enhancement has been found in many brain regions, including prefrontal cortex (Boch and Goldberg, 1987 Investigative Ophthalmology 28 Supplement, 124), V4 (Moran and Desimone, 1985 Science 229 782 – 784), and lateral intraparietal area (Colby et al, 1996 Journal of Neurophysiology 76 2841 – 2852; Colby and Goldberg, 1999 Annual Review of Neuroscience 22 319 – 349), and even V1 (Lamme et al, 2000 Vision Research 40 1507 – 1521). In these studies the assumption has been that the monkey attended to the stimulus because the stimulus evoked an enhanced response. In the experiments described here we show that for abruptly appearing stimuli, attention is not related to the initial response evoked by the stimulus, but by the activity present on the salience map in the parietal cortex when the stimulus appears. Attention to the stimulus may subsequently, by a top – down signal, sustain the map, but stimuli can as easily be suppressed by top – down features as they can be enhanced.

Feature attention evokes task-specific pattern selectivity in V4 neurons

A hallmark of visual cortical neurons is their selectivity for stimulus pattern features, such as color, orientation, or shape. In most cases this feature selectivity is hard-wired, with selectivity manifest from the beginning of the response. Here we show that when a task requires that a monkey distinguish between patterns, V4 develops a selectivity for the sought-after pattern, which it does not manifest in a task that does not require the monkey to distinguish between patterns. When a monkey looks for a target object among an array of distractors, V4 neurons become selective for the target ∼50 ms after the visual latency independent of the impending saccade direction. However, when the monkey has to only make a saccade to the spatial location of the same objects without discriminating their pattern, V4 neurons do not distinguish the search target from the distractors. This selectivity for stimulus pattern develops roughly 40 ms after the same neurons’ selectivity for basic pattern features like orientation or color. We suggest that this late-developing selectivity is related to the phenomenon of feature attention and may contribute to the mechanisms by which the brain finds the target in visual search.

Extrafoveal preview benefit during free-viewing visual search in the monkey

Previous studies have shown that subjects require less time to process a stimulus at the fovea after a saccade if they have viewed the same stimulus in the periphery immediately prior to the saccade. This extrafoveal preview benefit indicates that information about the visual form of an extrafoveally viewed stimulus can be transferred across a saccade. Here, we extend these findings by demonstrating and characterizing a similar extrafoveal preview benefit in monkeys during a free-viewing visual search task. We trained two monkeys to report the orientation of a target among distractors by releasing one of two bars with their hand; monkeys were free to move their eyes during the task. Both monkeys took less time to indicate the orientation of the target after foveating it, when the target lay closer to the fovea during the previous fixation. An extrafoveal preview benefit emerged even if there was more than one intervening saccade between the preview and the target fixation, indicating that information about target identity could be transferred across more than one saccade and could be obtained even if the search target was not the goal of the next saccade. An extrafoveal preview benefit was also found for distractor stimuli. These results aid future physiological investigations of the extrafoveal preview benefit.

Activity in V4 Reflects the Direction, But Not the Latency, of Saccades During Visual Search

We constantly make eye movements to bring objects of interest onto the fovea for more detailed processing. Activity in area V4, a prestriate visual area, is enhanced at the location corresponding to the target of an eye movement. However, the precise role of activity in V4 in relation to these saccades and the modulation of other cortical areas in the oculomotor system remains unknown. V4 could be a source of visual feature information used to select the eye movement, or alternatively, it could reflect the locus of spatial attention. To test these hypotheses, we trained monkeys on a visual search task in which they were free to move their eyes. We found that activity in area V4 reflected the direction of the upcoming saccade but did not predict the latency of the saccade in contrast to activity in the lateral intraparietal area (LIP). We suggest that the signals in V4, unlike those in LIP, are not directly involved in the generation of the saccade itself but rather are more closely linked to visual perception and attention. Although V4 and LIP have different roles in spatial attention and preparing eye movements, they likely perform complimentary processes during visual search.

Electrophysiological evidence for cerebellar involvement in higher-order cognitive processing

Although the cerebellum has been traditionally considered to be exclusively involved in motor control and learning, recent anatomical and clinical studies suggest that it may also have a role in cognition. However, no electrophysiological evidence exists to support this claim. Here we studied the activity of simple spikes of hand-movement related Purkinje cells in the mid-lateral cerebellum when monkeys learned to associate a well-learned right or left-hand movement with one of two visual symbolic cues. The cells had distinctly different discharge patterns between an overtrained symbol-hand association and a novel symbol-hand association although the kinematics of the movement did not change between the two conditions. The activity change was not related to the pattern of the visual symbols, the hand making the movement, the monkeys’ reaction times or the novelty of the visual symbols. We suggest that mid-lateral cerebellum is involved in higher-order cognitive processing related to learning a new visuomotor association. One Sentence Summary Hand-movement related Purkinje neurons in midlateral cerebellum, which discharge during an overtrained visuomotor association task, change their activity when the monkey has to associate the same movements with new cues, even though the kinematics of the movements do not change.