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. Based on our findings, we suggest that intrinsic timescales reflect areal specialization for task-relevant computations over multiple temporal ranges.
The ability to group stimuli into meaningful categories is a fundamental cognitive process. To explore its neural basis, we trained monkeys to categorize computer-generated stimuli as "cats" and "dogs." A morphing system was used to systematically vary stimulus shape and precisely define the category boundary. Neural activity in the lateral prefrontal cortex reflected the category of visual stimuli, even when a monkey was retrained with the stimuli assigned to new categories.
Deriving the quantity of items is an abstract form of categorization. To explore it, monkeys were trained to judge whether successive visual displays contained the same quantity of items. Many neurons in the lateral prefrontal cortex were tuned for quantity irrespective of the exact physical appearance of the displays. Their tuning curves formed overlapping filters, which may explain why behavioral discrimination improves with increasing numerical distance and why discrimination of two quantities with equal numerical distance worsens as their numerical size increases. A mechanism that extracts the quantity of visual field items could contribute to general numerical ability.
Categorization is a process by which the brain assigns meaning to sensory stimuli. Through experience, we learn to group stimuli into categories, such as 'chair', 'table' and 'vehicle', which are critical for rapidly and appropriately selecting behavioural responses. Although much is known about the neural representation of simple visual stimulus features (for example, orientation, direction and colour), relatively little is known about how the brain learns and encodes the meaning of stimuli. We trained monkeys to classify 360 degrees of visual motion directions into two discrete categories, and compared neuronal activity in the lateral intraparietal (LIP) and middle temporal (MT) areas, two interconnected brain regions known to be involved in visual motion processing. Here we show that neurons in LIP--an area known to be centrally involved in visuo-spatial attention, motor planning and decision-making-robustly reflect the category of motion direction as a result of learning. The activity of LIP neurons encoded directions of motion according to their category membership, and that encoding shifted after the monkeys were retrained to group the same stimuli into two new categories. In contrast, neurons in area MT were strongly direction selective but carried little, if any, explicit category information. This indicates that LIP might be an important nexus for the transformation of visual direction selectivity to more abstract representations that encode the behavioural relevance, or meaning, of stimuli.
Previous studies have suggested that both the prefrontal cortex (PFC) and inferior temporal cortex (ITC) are involved in high-level visual processing and categorization, but their respective roles are not known. To address this, we trained monkeys to categorize a continuous set of visual stimuli into two categories, "cats" and "dogs." The stimuli were parametrically generated using a computer graphics morphing system (Sheltonelton, 2000) that allowed precise control over stimulus shape. After training, we recorded neural activity from the PFC and the ITC of monkeys while they performed a category-matching task. We found that the PFC and the ITC play distinct roles in category-based behaviors: the ITC seems more involved in the analysis of currently viewed shapes, whereas the PFC showed stronger category signals, memory effects, and a greater tendency to encode information in terms of its behavioral meaning.
Most electrophysiology studies analyze the activity of each neuron separately. While such studies have given much insight into properties of the visual system, they have also potentially overlooked important aspects of information coded in changing patterns of activity that are distributed over larger populations of neurons. In this work, we apply a population decoding method to better estimate what information is available in neuronal ensembles and how this information is coded in dynamic patterns of neural activity in data recorded from inferior temporal cortex (ITC) and prefrontal cortex (PFC) as macaque monkeys engaged in a delayed match-to-category task. Analyses of activity patterns in ITC and PFC revealed that both areas contain "abstract" category information (i.e., category information that is not directly correlated with properties of the stimuli); however, in general, PFC has more task-relevant information, and ITC has more detailed visual information. Analyses examining how information coded in these areas show that almost all category information is available in a small fraction of the neurons in the population. Most remarkably, our results also show that category information is coded by a nonstationary pattern of activity that changes over the course of a trial with individual neurons containing information on much shorter time scales than the population as a whole.
The ability to generalize behaviour-guiding principles and concepts from experience is key to intelligent, goal-directed behaviour. It allows us to deal efficiently with a complex world and to adapt readily to novel situations. We review evidence that the prefrontal cortex-the cortical area that reaches its greatest elaboration in primates-plays a central part in acquiring and representing this information. The prefrontal cortex receives highly processed information from all major forebrain systems, and neurophysiological studies suggest that it synthesizes this into representations of learned task contingencies, concepts and task rules. In short, the prefrontal cortex seems to underlie our internal representations of the 'rules of the game'. This may provide the necessary foundation for the complex behaviour of primates, in whom this structure is most elaborate.
Whereas much is known about the visual shape selectivity of neurons in the inferior temporal cortex (ITC), less is known about the role of visual learning in the development and refinement of ITC shape selectivity. To address this, we trained monkeys to perform a visual categorization task with a parametric set of highly familiar stimuli. During training, the stimuli were always presented at the same orientation. In this experiment, we recorded from ITC neurons while monkeys viewed the trained stimuli in addition to image-plane rotated versions of those stimuli. We found that, concomitant with the monkeys' behavioral performance, neuronal stimulus selectivity was stronger for stimuli presented at the trained orientation than for rotated versions of the same stimuli. We also recorded from ITC neurons while monkeys viewed sets of novel and familiar (but not explicitly trained) randomly chosen complex stimuli. We again found that ITC stimulus selectivity was sharper for familiar than novel stimuli, suggesting that enhanced shape tuning in ITC can arise for both passively experienced and explicitly trained stimuli.
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