Paul S. Khayat

Different Processing Phases for Features, Figures, and Selective Attention in the Primary Visual Cortex

Our visual system imposes structure onto images that usually contain a diversity of surfaces, contours, and colors. Psychological theories propose that there are multiple steps in this process that occur in hierarchically organized regions of the cortex: early visual areas register basic features, higher areas bind them into objects, and yet higher areas select the objects that are relevant for behavior. Here we test these theories by recording from the primary visual cortex (area V1) of monkeys. We demonstrate that the V1 neurons first register the features (at a latency of 48 ms), then segregate figures from the background (after 57 ms), and finally select relevant figures over irrelevant ones (after 137 ms). We conclude that the psychological processing stages map onto distinct time episodes that unfold in the visual cortex after the presentation of a new stimulus, so that area V1 may contribute to all these processing steps.

Subtask sequencing in the primary visual cortex

Complex visual tasks can usually be decomposed into a number of simpler subtasks. Whether such subtasks are solved serially or in parallel is subject to considerable debate. Here we investigate how subtasks are coordinated in time by recording from the primary visual cortex of macaque monkeys. The animals were trained to perform both a simple and a composite task. In the simple task, they had to mentally trace a target curve while ignoring a distractor curve. Neuronal responses in the primary visual cortex to the target curve were enhanced relative to responses to the distractor curve 130 ms after stimulus appearance. In the composite task, the monkeys searched for a colored marker and traced a curve that was attached to this marker. In an initial phase of the trials, neuronal responses reflected visual search, and the response enhancement due to curve tracing now occurred after 230 ms, 100 ms later than in the simple task. We conclude that subtasks of the composite task are carried out in a structured and sequential manner that can be monitored in the primary visual cortex.

Neuronal Activity in the Visual Cortex Reveals the Temporal Order of Cognitive Operations

Most mental processes consist of a number of processing steps that are executed sequentially. The timing of the individual mental operations can usually only be estimated indirectly, from the pattern of reaction times. In vision, however, many processing steps are associated with the modulation of neuronal activity in early visual areas. Here we exploited this association to elucidate the time course of neuronal activity related to each of the self-paced mental processing steps in complex visual tasks. We trained monkeys to perform two tasks, search–trace and trace–search, which required performing a sequence of two operations: a visual search for a specific color and the mental tracing of a curve. We used multielectrode recording techniques to monitor the representations of multiple visual items in area V1 at the same time and found that the relevant curve as well as the target of visual search evoked enhanced neuronal activity with a timing that depended on the order of operations. This modulation of neuronal activity in early visual areas could allow these areas to (1) act as a cognitive blackboard that permits the exchange of information between successive processing steps of a sequential visual task and to (2) contribute to the orderly progression of task-dependent endogenous attention shifts that are driven by task structure and evolve over hundreds of milliseconds.

Time Course of Attentional Modulation in the Frontal Eye Field During Curve Tracing

Neurons in the frontal eye fields (FEFs) register incoming visual information and select visual stimuli that are relevant for behavior. Here we investigated the timing of the visual response and the timing of selection by recording from single FEF neurons in a curve-tracing task that requires shifts of attention followed by an oculomotor response. We found that the behavioral selection signal in area FEF had a latency of 147 ms and that it was delayed substantially relative to the visual response, which occurred 50 ms after stimulus presentation. We compared the FEF responses to activity previously recorded in the primary visual cortex (area V1) during the same task. Visual responses in area V1 preceded the FEF responses, but the latencies of selection signals in areas V1 and FEF were similar. The similarity of timing of selection signals in structures at opposite ends of the visual cortical processing hierarchy supports the view that stimulus selection occurs in an interaction between widely separated cortical regions.

Cellular response to texture and form defined by motion in area 19 of the cat.

The present study examined the neuronal sensitivity in area 19 of the cat to a motion‐defined bar and to texture. Sensitivity was tested in normal, lesioned (areas 17–18) and split‐chiasm cats using a kinematogram, as well as a textured bar drifting on a uniform light background and a light bar drifting on a stationary textured background. Texture density was varied. The results indicate that almost all cells of area 19 recorded in the three groups of cats responded to a motion‐defined bar or to its edges. Texture density influenced the responses in that the discharge rate increased as density decreased. However, the majority of cells were sensitive to the highest texture density kinematogram. Moreover, the neural responses of all cats were either independent of the density of the textured bar or background, or were modulated by it. These results show that cells in area 19 can signal the presence of a kinetic bar and that the density of either the textured bar, the background or both can influence figure–ground detection. The results are interpreted with respect to how various inputs influence the function of area 19.

Effects of attention and distractor contrast on the responses of middle temporal area neurons to transient motion direction changes.

The ability of primates to detect transient changes in a visual scene can be influenced by the allocation of attention, as well as by the presence of distractors. We investigated the neural substrates of these effects by recording the responses of neurons in the middle temporal area (MT) of two monkeys while they detected a transient motion direction change in a moving target. We found that positioning a distractor near the target impaired the change‐detection performance of the animals. This impairment monotonically decreased as the distractors contrast decreased. A neural correlate of this effect was a decrease in the ability of MT neurons to signal the direction change (detection sensitivity or DS) when a distractor was near the target, both located inside the neurons receptive field. Moreover, decreasing distractor contrast increased neuronal DS. On the other hand, directing attention away from the target decreased neuronal DS. At the level of individual neurons, we found a negative correlation between the degree of response normalization and the DS. Finally, the intensity of a neurons response to the change was predictive of the animals reaction time, suggesting that the activity of our recorded neurons was linked to the animals detection performance. Our results suggest that the ability of an MT neuron to signal a transient direction change is regulated by the degree of inhibitory drive into the cell. The presence of distractors, their contrast and the allocation of attention influence such inhibitory drive, therefore modulating the ability of the neurons to signal transient changes in stimulus features and consequently behavioral performance.

Distracter suppression dominates attentional modulation of responses to multiple stimuli inside middle temporal (MT) neuron's receptive field

Single‐cell studies in macaques have shown that attending to one of two stimuli, positioned inside a visual neurons receptive field (RF), modulates the neurons response to reflect the features of the attended stimulus. Such a modulation has been described as a ‘push–pull’ effect relative to a reference response: a neurons response increases when attention is directed to a preferred stimulus, and decreases when attention is directed to a non‐preferred stimulus. It has been further suggested that the response increase when attending to a preferred stimulus is the predominant effect. Here, we show that the observed attentional modulation depends on the reference response. We recorded neuronal responses in motion processing area middle temporal (MT) of macaques to two moving random dot patterns positioned inside neurons’ RF. One pattern always moved in the neurons antipreferred direction (null pattern), while the other moved in one of 12 directions (tuning pattern). At the beginning of a trial, a cue indicated the location and direction of the target. The animal was required to release a lever when a change in the target direction occurred, and to ignore changes in the distracter. Relative to neurons’ initial responses to the dual stimuli (when attention was less likely to modulate responses), attending to the tuning pattern did not significantly modulate responses over time. However, attending to the null pattern progressively decreased responses over time. These results were quantitatively described by filter and input gain models, characterising a predominant response suppression relative to a reference response, rather than response enhancement.

A metric-based analysis of the contribution of spike timing to contrast and motion direction coding by single neurons in macaque area MT

Spike timing is thought to contribute to the coding of motion direction information by neurons in macaque area MT. Here, we examined whether spike timing also contributes to the coding of stimulus contrast. We applied a metric-based approach to spike trains fired by MT neurons in response to stimuli that varied in contrast, or direction. We assessed the performance of three metrics, D(spike) and D(product) (containing spike count and timing information), and the spike count metric D(count). We analyzed responses elicited during the first 200 msec of stimulus presentation from 205 neurons. For both contrast and direction, the large majority of neurons showed the highest mutual information using D(spike), followed by D(product), and D(count). This was corroborated by the performance of a theoretical observer model at discriminating contrast and direction using the three metrics. Our results demonstrate that spike timing can contribute to contrast coding in MT neurons, and support previous reports of its potential contribution to direction coding. Furthermore, they suggest that a combination of spike count with periodic and non-periodic spike timing information (contained in D(spike), but not in D(product) and D(count) which are insensitive to spike counts and timing respectively) provides the largest coding advantage in spike trains fired by MT neurons during contrast and direction discrimination.