Information about external stimuli is thought to be stored in cortical circuits through experience-dependent modifications of synaptic connectivity. These modifications of network connectivity should lead to changes in neuronal activity, as a particular stimulus is repeatedly encountered. Here, we ask what plasticity rules are consistent with the differences in the statistics of the visual response to novel and familiar stimuli in inferior temporal cortex, an area underlying visual object recognition. We introduce a method that allows inferring the dependence of the ‘learning rule’ on post-synaptic firing rate, and show that the inferred learning rule exhibits depression for low post-synaptic rates and potentiation for high rates. The threshold separating depression from potentiation is strongly correlated with both mean and standard deviation of the firing rate distribution. Finally, we show that network models implementing a rule extracted from data show stable learning dynamics, and lead to sparser representations of stimuli.

Primates can learn to recognize a virtually limitless number of visual objects. A candidate neural substrate for this adult plasticity is the inferior temporal cortex (ITC). Using a large stimulus set, we explored the impact that long-term experience has on the response properties of two classes of neurons in ITC, broad-spiking (putative excitatory) cells and narrow-spiking (putative inhibitory) cells. We found that experience increased maximum responses of putative excitatory neurons but had the opposite effect on maximum responses of putative inhibitory neurons, an observation that helps to reconcile contradictory reports regarding the presence and direction of this effect. In addition, we found that experience reduced the average stimulus-evoked response in both cell classes, but this decrease was much more pronounced in putative inhibitory units. This latter finding supports a potentially critical role of inhibitory neurons in detecting and initiating the cascade of events underlying adult neural plasticity in ITC.

Intelligent organisms are capable of tracking objects even when they temporarily disappear from sight, a cognitive capacity commonly referred to as visual working memory (VWM). The neural basis of VWM has been the subject of significant scientific debate, with recent work focusing on the relative roles of posterior visual areas, such as the inferior temporal cortex (ITC), and the prefrontal cortex. Here we reexamined the contribution of ITC to VWM by recording from highly selective individual ITC neurons as monkeys engaged in multiple versions of an occlusion-based memory task. As expected, we found strong evidence for a role of ITC in stimulus encoding. We also found that almost half of these selective cells showed stimulus-selective delay period modulation, with a small but significant fraction exhibiting differential responses even in the presence of simultaneously visible interfering information. When we combined the informational content of multiple neurons, we found that the accuracy with which we could decode memory content increased drastically. The memory epoch analyses suggest that behaviorally relevant visual memories were reinstated in ITC. Furthermore, we observed a population-wide enhancement of neuronal response to a match stimulus compared with the same stimulus presented as a nonmatch. The single-cell enhancement preceded any match effects identified in the local field potential, leading us to speculate that enhancement is the result of neural processing local to ITC. Moreover, match enhancement was only later followed by the more commonly observed match suppression. Altogether, the data support the hypothesis that, when a stimulus is held in memory, ITC neurons are actively biased in favor of task-relevant visual representations and that this bias can immediately impact subsequent recognition events.

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