Jude F. Mitchell

Differential Attention-Dependent Response Modulation across Cell Classes in Macaque Visual Area V4

The cortex contains multiple cell types, but studies of attention have not distinguished between them, limiting understanding of the local circuits that transform attentional feedback into improved visual processing. Parvalbumin-expressing inhibitory interneurons can be distinguished from pyramidal neurons based on their briefer action potential durations. We recorded neurons in area V4 as monkeys performed an attention-demanding task. We find that the distribution of action potential durations is strongly bimodal. Neurons with narrow action potentials have higher firing rates and larger attention-dependent increases in absolute firing rate than neurons with broad action potentials. The percentage increase in response is similar across the two classes. We also find evidence that attention increases the reliability of the neuronal response. This modulation is more than two-fold stronger among putative interneurons. These findings lead to the surprising conclusion that the strongest attentional modulation occurs among local interneurons that do not transmit signals between areas.

Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4

Attention typically amplifies neuronal responses evoked by task-relevant stimuli while attenuating responses to task-irrelevant distracters. In this context, visual distracters constitute an external source of noise that is diminished to improve attended signal quality. Activity that is internal to the cortex itself, stimulus-independent ongoing correlated fluctuations in firing, might also act as task-irrelevant noise. To examine this, we recorded from area V4 of macaques performing an attention-demanding task. The firing of neurons to identically repeated stimuli was highly variable. Much of this variability originates from ongoing low-frequency (<5 Hz) fluctuations in rate correlated across the neuronal population. When attention is directed to a stimulus inside a neurons receptive field, these correlated fluctuations in rate are reduced. This attention-dependent reduction of ongoing cortical activity improves the signal-to-noise ratio of pooled neural signals substantially more than attention-dependent increases in firing rate.

Object-based attention determines dominance in binocular rivalry

A question of long-standing interest to philosophers, psychologists and neuroscientists is how the brain selects which signals enter consciousness. Binocular rivalry and attention both involve selection of visual stimuli, but affect perception quite differently. During binocular rivalry, awareness alternates between two different stimuli presented to the two eyes. In contrast, attending to one of two different stimuli impairs discrimination of the ignored stimulus, but without causing it to disappear from consciousness. Here we show that despite this difference, attention and rivalry rely on shared object-based selection mechanisms. We cued attention to one of two superimposed transparent surfaces and then deleted the image of one surface from each eye, resulting in rivalry. Observers usually reported seeing only the cued surface. They were also less accurate in judging unpredictable changes in the features of the uncued surface. Our design ensured that selection of the cued surface could not have resulted from spatial, ocular or feature-based mechanisms. Rather, attention was drawn to one surface, and this caused the other surface to be perceptually suppressed during rivalry. These results raise the question of how object representations compete during these two forms of perceptual selection, even as the features of those objects change unpredictably over time.

Spatial Attention Modulates Center-Surround Interactions in Macaque Visual Area V4

In natural viewing, a visual stimulus that is the target of attention is generally surrounded by many irrelevant distracters. Stimuli falling in the receptive field surround can influence the neuronal response evoked by a stimulus appearing within the classical receptive field. Such modulation by task-irrelevant distracters may degrade the target-related neuronal signal. We therefore examined whether directing attention to a target stimulus can reduce the influence of task-irrelevant distracters on neuronal response. We find that in area V4 attention to a stimulus within a neurons receptive field filters out a large fraction of the suppression induced by distracters appearing in the surround. When attention is instead directed to the surround stimulus, suppression is increased, thereby filtering out part of the neuronal response to the irrelevant distracter positioned within the receptive field. These findings demonstrate that attention modulates the neural mechanisms that give rise to center-surround interactions.

Exogenous attentional selection of transparent superimposed surfaces modulates early event-related potentials.

Using a transparent motion paradigm, [Valdes-Sosa, M., Bobes, M. A., Rodriguez, V., & Pinilla, T. (1998). Switching attention without shifting the spotlight object-based attentional modulation of brain potentials, Journal of Cognitive Neuroscience, 10, 137-151; Valdes-Sosa, M., Cobo, A., & Pinilla, T. (2000). Attention to object files defined by transparent motion, Journal of Experimental Psychological: Human Perception and Performance, 26, 488-505] found that when attention is endogenously directed to one surface, observers can more reliably report the direction of a brief translation of the cued than the uncued surface. Using a similar design [Reynolds, J. H., Alborzian, S., & Stoner, G. R. (2003). Exogenously cued attention triggers competitive selection of surfaces, Vision Research, 43, 59-66] found that even in the absence of an endogenous cue, the first translation acted as a potent exogenous cue that impaired the observers ability to discriminate a subsequent translation of the other surface. We investigated the neural basis of this exogenous cueing effect by recording visual event-related potentials (ERPs) elicited by translations of the cued and uncued surfaces. Subjects were given the task of judging whether or not the first and second translations were identical in direction, and their performance was impaired when the second translation occurred on the uncued, as compared to the cued surface. The posterior C1 (75-110 ms) and N1 (160-210 ms) components of the ERP elicited by the second translation of the cued surface were larger than those elicited by translation of the uncued surface. These behavioral and ERP cueing effects were present even when the two surfaces were identical in color and thus could not be attributed to attention-related modulations of the gain of color channels. These findings provide evidence that exogenous cueing results in preferential selection of the cued surface at both early and intermediate stages of visual-cortical processing.

Active Vision in Marmosets: A Model System for Visual Neuroscience

The common marmoset (Callithrix jacchus), a small-bodied New World primate, offers several advantages to complement vision research in larger primates. Studies in the anesthetized marmoset have detailed the anatomy and physiology of their visual system (Rosa et al., 2009) while studies of auditory and vocal processing have established their utility for awake and behaving neurophysiological investigations (Lu et al., 2001a,b; Eliades and Wang, 2008a,b; Osmanski and Wang, 2011; Remington et al., 2012). However, a critical unknown is whether marmosets can perform visual tasks under head restraint. This has been essential for studies in macaques, enabling both accurate eye tracking and head stabilization for neurophysiology. In one set of experiments we compared the free viewing behavior of head-fixed marmosets to that of macaques, and found that their saccadic behavior is comparable across a number of saccade metrics and that saccades target similar regions of interest including faces. In a second set of experiments we applied behavioral conditioning techniques to determine whether the marmoset could control fixation for liquid reward. Two marmosets could fixate a central point and ignore peripheral flashing stimuli, as needed for receptive field mapping. Both marmosets also performed an orientation discrimination task, exhibiting a saturating psychometric function with reliable performance and shorter reaction times for easier discriminations. These data suggest that the marmoset is a viable model for studies of active vision and its underlying neural mechanisms.

The marmoset monkey as a model for visual neuroscience

The common marmoset (Callithrix jacchus) has been valuable as a primate model in biomedical research. Interest in this species has grown recently, in part due to the successful demonstration of transgenic marmosets. Here we examine the prospects of the marmoset model for visual neuroscience research, adopting a comparative framework to place the marmoset within a broader evolutionary context. The marmosets small brain bears most of the organizational features of other primates, and its smooth surface offers practical advantages over the macaque for areal mapping, laminar electrode penetration, and two-photon and optical imaging. Behaviorally, marmosets are more limited at performing regimented psychophysical tasks, but do readily accept the head restraint that is necessary for accurate eye tracking and neurophysiology, and can perform simple discriminations. Their natural gaze behavior closely resembles that of other primates, with a tendency to focus on objects of social interest including faces. Their immaturity at birth and routine twinning also makes them ideal for the study of postnatal visual development. These experimental factors, together with the theoretical advantages inherent in comparing anatomy, physiology, and behavior across related species, make the marmoset an excellent model for visual neuroscience.

The Fine Structure of Shape Tuning in Area V4

Previous studies have shown that neurons in area V4 are involved in the processing of shapes of intermediate complexity and are sensitive to curvature. These studies also suggest that curvature-tuned neurons are position invariant. We sought to examine the mechanisms that endow V4 neurons with these properties. Consistent with previous studies, we found that response rank order to the most- and least-preferred stimuli was preserved throughout the receptive field. However, a fine-grained analysis of shape tuning revealed a surprising result: V4 neurons tuned to highly curved shapes exhibit very limited translation invariance. At a fine spatial scale, these neurons exhibit local variation in orientation. In contrast, neurons that prefer straight contours exhibit spatially invariant orientation-tuning and homogenous fine-scale orientation maps. Both of these patterns are consistent with a simple orientation-pooling model, with tuning for straight or curved shapes resulting, respectively, from pooling of homogenous or heterogeneous orientation signals inherited from early visual areas.

Attention influences single unit and local field potential response latencies in visual cortical area V4.

Many previous studies have demonstrated that changes in selective attention can alter the response magnitude of visual cortical neurons, but there has been little evidence for attention affecting response latency. Small latency differences, though hard to detect, can potentially be of functional importance, and may also give insight into the mechanisms of neuronal computation. We therefore reexamined the effect of attention on the response latency of both single units and the local field potential (LFP) in primate visual cortical area V4. We find that attention does produce small (1–2 ms) but significant reductions in the latency of both the spiking and LFP responses. Though attention, like contrast elevation, reduces response latencies, we find that the two have different effects on the magnitude of the LFP. Contrast elevations increase and attention decreases the magnitude of the initial deflection of the stimulus-evoked LFP. Both contrast elevation and attention increase the magnitude of the spiking response. We speculate that latencies may be reduced at higher contrast because stronger stimulus inputs drive neurons more rapidly to spiking threshold, while attention may reduce latencies by placing neurons in a more depolarized state closer to threshold before stimulus onset.

Attentional selection of superimposed surfaces cannot be explained by modulation of the gain of color channels.

When two differently colored, superimposed patterns of dots rotate in opposite directions, this yields the percept of two superimposed transparent surfaces. If observers are cued to attend to one set of dots, they are impaired in making judgments about the other set. Since the two sets of dots are overlapping, the cueing effect cannot be explained by spatial attention. This has led to the interpretation that the impairment reflects surface-based attentional selection. However, recent single-unit recording studies in monkeys have found that attention can modulate the gain of neurons tuned for features such as color. Thus, rather than reflecting the selection of a surface, the behavioral effects might simply reflect a reduction in the gain of color channels selective for the color of the uncued set of dots (feature-based attention), as if viewing the surfaces through a colored filter. If so, then the impairment should be eliminated when the two surfaces are made the same color. Instead, we find that the impairment persists with no reduction in strength. Our findings thus rule out the color gain explanation.