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

Abstract

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 to 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.

Linking neural activity to complex decisions

“…Because during this task we used both small and large differences between S1 and S2 directions, we were able to show that the magnitude of comparison effects decreased as the two directions became more similar (Fig 2C). This relationship paralleled behaviorally measured accuracy of direction discrimination and we found that comparison effect was no longer present for pairs of directions that the monkeys were unable to discriminate reliably (Hussar & Pasternak, 2012). This relationship between comparison effect and discrimination performance was further confirmed by finding lower incidence of comparison effects in the monkey with less accurate direction discrimination (see figs 7D & E in (Hussar & Pasternak, 2012)).…”

“…This relationship paralleled behaviorally measured accuracy of direction discrimination and we found that comparison effect was no longer present for pairs of directions that the monkeys were unable to discriminate reliably (Hussar & Pasternak, 2012). This relationship between comparison effect and discrimination performance was further confirmed by finding lower incidence of comparison effects in the monkey with less accurate direction discrimination (see figs 7D & E in (Hussar & Pasternak, 2012)). It is noteworthy, that we observed similar effects during an analogous task involving comparisons of stimulus speeds (Hussar & Pasternak, 2013b).…”

“…Recordings were carried out during a task that was similar to that used during MT recordings (Hussar & Pasternak, 2012). In the task used to probe DLPFC, the monkeys also compared two sequentially moving random dots that moved in the same or different directions.…”

“…Recordings in the DLPFC revealed that its contribution to motion comparisons is also not limited to a single component of the task. Rather, its neurons participate in all phases of the task, faithfully representing behaviorally relevant motion, showing stimulus-related and anticipatory activity during the delay, and representing the difference between the two comparison stimuli (Hussar & Pasternak, 2009; Hussar & Pasternak, 2010; Hussar & Pasternak, 2012; Hussar & Pasternak, 2013a). Thus, our data point to similarities in the way MT and DLPFC neurons represent behaviorally relevant visual motion and in the nature of their activity during the comparison phase of the task.…”

Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex

“…Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex. J Neurophysiol 108: 2725-2736, 2012. First published August 29, 2012 doi:10.1152/jn.00618.2012.-The cerebral cortex is composed of many distinct classes of neurons.…”