Natasha Sigala

Visual categorization shapes feature selectivity in the primate temporal cortex

The way that we perceive and interact with objects depends on our previous experience with them. For example, a bird expert is more likely to recognize a bird as a sparrow, a sandpiper or a cockatiel than a non-expert. Neurons in the inferior temporal cortex have been shown to be important in the representation of visual objects; however, it is unknown which object features are represented and how these representations are affected by categorization training. Here we show that feature selectivity in the macaque inferior temporal cortex is shaped by categorization of objects on the basis of their visual features. Specifically, we recorded from single neurons while monkeys performed a categorization task with two sets of parametric stimuli. Each stimulus set consisted of four varying features, but only two of the four were important for the categorization task (diagnostic features). We found enhanced neuronal representation of the diagnostic features relative to the non-diagnostic ones. These findings demonstrate that stimulus features important for categorization are instantiated in the activity of single units (neurons) in the primate inferior temporal cortex.

Dynamic Coding for Cognitive Control in Prefrontal Cortex

Summary Cognitive flexibility is fundamental to adaptive intelligent behavior. Prefrontal cortex has long been associated with flexible cognitive function, but the neurophysiological principles that enable prefrontal cells to adapt their response properties according to context-dependent rules remain poorly understood. Here, we use time-resolved population-level neural pattern analyses to explore how context is encoded and maintained in primate prefrontal cortex and used in flexible decision making. We show that an instruction cue triggers a rapid series of state transitions before settling into a stable low-activity state. The postcue state is differentially tuned according to the current task-relevant rule. During decision making, the response to a choice stimulus is characterized by an initial stimulus-specific population response but evolves to different final decision-related states depending on the current rule. These results demonstrate how neural tuning profiles in prefrontal cortex adapt to accommodate changes in behavioral context. Highly flexible tuning could be mediated via short-term synaptic plasticity.

Hierarchical coding for sequential task events in the monkey prefrontal cortex

The frontal lobes play a key role in sequential organization of behavior. Little is known, however, of the way frontal neurons code successive phases of a structured task plan. Using correlational analysis, we asked how a population of frontal cells represents the multiple events of a complex sequential task. Monkeys performed a conventional cue–target association task, with distinct cue, delay, and target phases. Across the population of recorded cells, we examined patterns of activity for different task phases, and in the same phase, for different stimulus objects. The results show hierarchical representation of task events. For different task phases, there were different, approximately orthogonal patterns of activity across the population of neurons. Modulations of each basic pattern encoded stimulus information within each phase. By orthogonal coding, the frontal lobe may control transitions between the discrete steps of a mental program; by correlated coding within each step, similar operations may be applied to different stimulus content.

Visual Categorization and Object Representation in Monkeys and Humans

We investigated the influence of a categorization task on the extraction and representation of perceptual features in humans and monkeys. The use of parameterized stimuli (schematic faces and fish) with fixed diagnostic features in combination with a similarity-rating task allowed us to demonstrate perceptual sensitization to the diagnostic dimensions of the categorization task for the monkeys. Moreover, our results reveal important similarities between human and monkey visual subordinate categorization strategies. Neither the humans nor the monkeys compared the new stimuli to class prototypes or based their decisions on conditional probabilities along stimulus dimensions. Instead, they classified each object according to its similarity to familiar members of the alternative categories, or with respect to its position to a linear boundary between the learned categories.

The neural mechanisms of object working memory: what is where in the infant brain?

The question of how representational capacities develop in humans has been engaging cognitive psychologists for decades. Looking time studies have explored when infants start to show signs of perceiving and remembering the properties of specific objects at specific locations. Here we integrate these findings into the neuroscientific framework of human visual working memory. We suggest that the development of a system involving the temporal cortex, thalamic and hippocampal structures and possibly the dorsolateral prefrontal cortex (later in development) can account for these behavioral results. Our explanation differs from most of the current approaches in developmental science as we put less emphasis on the contribution of lateral prefrontal areas. We discuss shortcomings of the theories that propose a functional subdivision of these areas and their difficulty in accounting for results from monkey lesion and infant studies. We believe that this shift in focus is desirable both in light of what recent results on medial temporal lobe processing reveal about object working memory, and given how well these results fit the behavioral developmental data.

Visual categorization and the inferior temporal cortex

We investigated the effects of categorization on the representation of stimulus features in combined psychophysical-electrophysiological experiments. We used parameterized line drawings of faces and fish as stimuli, and we varied the relevance of the different features for the categorization task. The psychophysical and electrophysiological data support an exemplar-based framework for visual object recognition. We recorded from visual neurons in the anterior inferior temporal (IT) cortex of macaque monkeys, while they were performing a categorization task. The visual neurons did not respond selectively to one stimulus set, or to one category. The majority of the anterior IT feature selective neurons were tuned for features that were diagnostic for the categorization task. We argue that this fine-tuning of the neurons reflects the perceptual sensitization to the diagnostic features.

Detection of Fixed and Variable Targets in the Monkey Prefrontal Cortex

Behavioral significance is commonly coded by prefrontal neurons. The significance of a stimulus can be fixed through experience; in complex behavior, however, significance commonly changes with short-term context. To compare these cases, we trained monkeys in 2 versions of visual target detection. In both tasks, animals monitored a series of pictures, making a go response (saccade) at the offset of a specified target picture. In one version, based on “consistent mapping” in human visual search, target and nontarget pictures were fixed throughout training. In the other, based on “varied mapping,” a cue at trial onset defined a new target. Building up over the first 1 s following this cue, many cells coded short-term context (cue/target identity) for the current trial. Thereafter, the cell population showed similar coding of behavioral significance in the 2 tasks, with selective early response to targets, and later, sustained activity coding target or nontarget until response. This population similarity was seen despite quite different activity in the 2 tasks for many single cells. At the population level, the results suggest similar prefrontal coding of fixed and short-term behavioral significance.

Dynamic Construction of a Coherent Attentional State in a Prefrontal Cell Population

Summary Prefrontal cortex has been proposed to show highly adaptive information coding, with neurons dynamically allocated to processing task-relevant information. To track this dynamic allocation in monkey prefrontal cortex, we used time-resolved measures of neural population activity in a simple case of competition between target (behaviorally critical) and nontarget objects in opposite visual hemifields. Early in processing, there were parallel responses to competing inputs, with neurons in each hemisphere dominated by the contralateral stimulus. Later, the nontarget lost control of neural activity, with emerging global control by the behaviorally critical target. The speed of transition reflected the competitive weights of different display elements, occurring most rapidly when relative behavioral significance was well established by training history. In line with adaptive coding, the results show widespread reallocation of prefrontal processing resources as an attentional focus is established.

Evidence for long-range feedback in target detection: Detection of semantic targets modulates activity in early visual areas

In a variety of attention and search tasks, single-cell recordings of the primate brain have frequently shown an enhancement of responses in early visual areas to selected target stimuli. This enhancement is observed only at longer latencies, suggesting the possibility that it reflects the action of feedback or return signals from upstream processing areas. However, in typical studies, targets are specified on the basis of elementary visual features; as these are coded at multiple levels of the visual system, it is impossible to determine where enhanced target processing begins. Using human functional magnetic resonance imaging (fMRI), we demonstrate enhancement of activity in early visual areas even when low-level visual information is insufficient for target detection to occur. We found enhanced activity in early visual areas to targets defined purely by semantic category, suggesting that feedback signals returning from at least as far forward as temporal lobe semantic processing can influence visual responses. These findings also suggest feedback signaling as a mechanism by which early and late brain systems coding for different properties of a target object can integrate their activity, allowing for the target object to dominate overall processing.

Target detection by opponent coding in monkey prefrontal cortex

The pFC plays a key role in flexible, context-specific decision making. One proposal [Machens, C. K., Romo, R., & Brody, C. D. Flexible control of mutual inhibition: A neural model of two-interval discrimination. Science, 307, 1121–1124, 2005] is that prefrontal cells may be dynamically organized into opponent coding circuits, with competitive groups of cells coding opposite behavioral decisions. Here, we show evidence for extensive, temporally evolving opponent organization in the monkey pFC during a cued target detection task. More than a half of all randomly selected cells discriminated stimulus category in this task. The largest set showed target-positive activity, with the strongest responses to the current target, intermediate activity for a nontarget that was a target on other trials, and lowest activity for nontargets never associated with the target category. Second most frequent was a reverse, antitarget pattern. In the ventrolateral frontal cortex, opponent organization was strongly established in phasic responses at stimulus onset; later, such activity was widely spread across dorsolateral and ventrolateral sites. Task-specific organization into opponent cell groups may be a general feature of prefrontal decision making.