Tatiana Pasternak

Attention increases sensitivity of V4 neurons.

When attention is directed to a location in the visual field, sensitivity to stimuli at that location is increased. At the neuronal level, this could arise either through a multiplicative increase in firing rate or through an increase in the effective strength of the stimulus. To test conflicting predictions of these alternative models, we recorded responses of V4 neurons to stimuli across a range of luminance contrasts and measured the change in response when monkeys attended to them in order to discriminate a target stimulus from nontargets. Attention caused greater increases in response at low contrast than at high contrast, consistent with an increase in effective stimulus strength. On average, attention increased the effective contrast of the attended stimulus by a factor of 1.51, an increase of 51% of its physical contrast.

Working memory in primate sensory systems

Sensory working memory consists of the short-term storage of sensory stimuli to guide behaviour. There is increasing evidence that elemental sensory dimensions — such as object motion in the visual system or the frequency of a sound in the auditory system — are stored by segregated feature-selective systems that include not only the prefrontal and parietal cortex, but also areas of sensory cortex that carry out relatively early stages of processing. These circuits seem to have a dual function: precise sensory encoding and short-term storage of this information. New results provide insights into how activity in these circuits represents the remembered sensory stimuli.

A hierarchy of intrinsic timescales across primate cortex

Specialization and hierarchy are organizing principles for primate cortex, yet there is little direct evidence for how cortical areas are specialized in the temporal domain. We measured timescales of intrinsic fluctuations in spiking activity across areas and found a hierarchical ordering, with sensory and prefrontal areas exhibiting shorter and longer timescales, respectively. On the basis of our findings, we suggest that intrinsic timescales reflect areal specialization for task-relevant computations over multiple temporal ranges.

Directional Signals in the Prefrontal Cortex and in Area MT during a Working Memory for Visual Motion Task

Neurons in the middle temporal visual area (MT) have been implicated in the perception of visual motion, whereas prefrontal cortex (PFC) neurons have been linked to temporary storage of sensory signals, attentional and executive control of behavior. Using a task that placed demands on both sets of neurons, we investigated their contribution to working memory for visual motion. Monkeys compared the direction of two moving random-dot stimuli, sample and test, separated by a brief memory delay. Neurons in both areas showed robust direction-selective activity during all phases of the task. During the sample, ∼60% of task-related PFC neurons were direction selective, and this selectivity emerged 40 ms later than in MT. Unlike MT, the PFC responses to sample did not correlate with behavioral choices, but their selectivity was modulated by task demands and diminished on error trials. Reliable directional signals were found in both areas during the memory delay, but these signals were transient rather than sustained by neurons of either area. Responses to the test in both areas were modulated by the remembered sample direction, decreasing when the test direction matched the sample. This decrease arose in the PFC 100 ms later than in MT and was predictive of the forthcoming decision. Our data suggest that neurons in the two regions are functionally connected and make unique contributions to different task components. PFC neurons reflect task-related information about visual motion and represent decisions that may be based, in part, on the comparison in MT between the remembered sample and test.

The luminance dependence of spatial vision in the cat.

The spatial contrast sensitivity and spatial resolution of three cats and one human observer were measured behaviorally over a 6 log unit range of luminances. At the highest luminance tested (16 cd/m2), cats showed lower peak contrast sensitivity than humans and their sensitivity function was located at lower spatial frequencies. As luminance was reduced, the contrast sensitivity of both humans and cats declined while both peak sensitivity and the limit of resolution shifted toward lower frequencies. These changes were more pronounced in humans and resulted in a convergence of both contrast sensitivity and spatial resolution of the two species at the lowest luminance tested. The dissimilarities in the luminance dependence of spatial vision in cats and humans appear to be due to differences in both photoreceptor distribution and receptor-ganglion cell convergence.

Flexibility of Sensory Representations in Prefrontal Cortex Depends on Cell Type

Discrimination tasks require processing, interpreting, and linking sensory information to the appropriate motor response. We report that neurons in prefrontal cortex (PFC) represent visual motion with precision comparable to cortical neurons at early stages of motion processing, and readily adapt this representation to behavioral context. We found that direction selectivity, recorded while the monkeys discriminated directions, decreased when they judged motion speed and ignored its direction. This decrease was more pronounced in neurons classified as narrow-spiking (NS) putative interneurons than in broad-spiking (BS) putative pyramidal neurons. However, during passive fixation, when the link between motion and its behavioral relevance was removed, both cell types showed a severe selectivity loss. Our results show that flexible sensory representation during active discrimination tasks is achieved in the PFC by a specialized neuronal network of both NS neurons readily adjusting their selectivity to behavioral context, and BS neurons capable of maintaining relatively stable sensory representation.

Deficits in speed discrimination following lesions of the lateral suprasylvian cortex in the cat

We examined the role of the lateral suprasylvian (LS) cortex in motion perception by testing the ability of three cats to detect moving targets and to discriminate differences in stimulus direction and speed before and after making bilateral ibotenic acid lesions in LS. The lesions had little or no effect on contrast sensitivity for detecting moving sinusoidal gratings. Moreover, we found no deficits in discriminating opposite directions of motion: the cats discriminated grating directions at threshold contrasts. All three cats, however, showed permanent deficits in discriminating differences in speed and in flicker rate. The deficits were most pronounced at higher temporal and spatial frequencies and at lower contrasts. This result suggests that LS plays an important role in the analysis of stimulus speed. It appears that information needed for discriminating opposite directions of motion may be signalled by visual areas outside LS.

Trial-to-trial variability of the prefrontal neurons reveals the nature of their engagement in a motion discrimination task

During motion discrimination tasks, many prefrontal cortex (PFC) neurons are strongly modulated by the behavioral context, suggesting their involvement in sensory discriminations. Recent studies suggest that trial-to-trial variability of spiking activity characteristic of cortical neurons could be a source of information about the state of neurons and their participation in behavioral tasks. We tested this hypothesis by examining the variability of putative pyramidal PFC neurons, a likely source of top-down influences. The variability of these neurons was calculated as a ratio of spike count variance to its mean (fano factor, FF), while monkeys compared the directions of two moving stimuli, sample and test, separated by a delay. We found that the FF tracked consecutive components of the task, dropping rapidly with the onset of stimuli being discriminated and declining more slowly before each salient event of the trial: The sample, the test, and the response. These time-dependent signals were less consistent in direction selective neurons and were largely absent during passive fixation. Furthermore, neurons with test responses that reflected the remembered sample decreased their FF well before the test, revealing the predictive nature of response variability, an effect present only during the active task. The FF was also sensitive to behavioral performance, exhibiting different temporal dynamics on error trials. These changes did not depend on firing rates and were often the only metric correlated with task demands. Our results demonstrate that trial-to-trial variability provides a sensitive measure of the engagement of putative pyramidal PFC neurons in circuits subserving discrimination tasks.

Memory-Guided Sensory Comparisons in the Prefrontal Cortex: Contribution of Putative Pyramidal Cells and Interneurons

Comparing two stimuli that occur at different times demands the coordination of bottom-up and top-down processes. It has been hypothesized that the dorsolateral prefrontal (PFC) cortex, the likely source of top-down cortical influences, plays a key role in such tasks, contributing to both maintenance and sensory comparisons. We examined this hypothesis by recording from the PFC of monkeys comparing directions of two moving stimuli, S1 and S2, separated by a memory delay. We determined the contribution of the two principal cell types to these processes by classifying neurons into broad-spiking (BS) putative pyramidal cells and narrow-spiking (NS) putative local interneurons. During the delay, BS cells were more likely to exhibit anticipatory modulation and represent the remembered direction. While this representation was transient, appearing at different times in different neurons, it weakened when direction was not task relevant, suggesting its utility. During S2, both putative cell types showed comparison-related activity modulations. These modulations were of two types, each carried by different neurons, which either preferred trials with stimuli moving in the same direction or trials with stimuli of different directions. These comparison effects were strongly correlated with choice, suggesting their role in circuitry underlying decision making. These results provide the first demonstration of distinct contributions made by principal cell types to memory-guided perceptual decisions. During sensory stimulation both cell types represent behaviorally relevant stimulus features contributing to comparison and decision-related activity. However in the absence of sensory stimulation, putative pyramidal cells dominated, carrying information about the elapsed time and the preceding direction.

Discrimination of differences in speed and flicker rate depends on directionally selective mechanisms

The present study compared discriminations of differences in speed to differences in temporal frequency and examined the role of directionally selective mechanisms in such discriminations. In measuring the contrast dependence of speed and temporal frequency discriminations two different techniques were used to reduce the role of directionally selective mechanisms. The first was the virtual elimination of directional selectivity in the visual cortex of cats by stroboscopic rearing. The second was the reduction of directional sensitivity in normal humans and cats by testing with gratings of high spatial and low temporal frequency. Discrimination of the temporal frequency of sinusoidal gratings flickered in counterphase was worse than discrimination of speeds of moving gratings. Under conditions that maximize the sensitivity of directional mechanisms (low spatial, moderate temporal frequency) Weber fractions for speed and flicker in all normal observers (cats and humans) were constant at higher contrast and increased only as contrast began to approach threshold. In strobe-reared cats sensitivity for direction was 10 times lower than sensitivity for detection. They were able to discriminate speeds and temporal frequencies only at contrasts that exceeded contrast threshold for direction. This was also true for a normal cat whose sensitivity for direction was reduced by increasing the spatial frequency of the grating. In all cases Weber fractions for flicker as a function of contrast were greater than but paralleled those for speed.