A dominant theory of working memory (WM), referred to as the persistent activity hypothesis, holds that recurrently connected neural networks, presumably located in the prefrontal cortex, encode and maintain WM memory items through sustained elevated activity. Reexamination of experimental data has shown that prefrontal cortex activity in single units during delay periods is much more variable than predicted by such a theory and associated computational models. Alternative models of WM maintenance based on synaptic plasticity, such as short-term nonassociative (non-Hebbian) synaptic facilitation, have been suggested but cannot account for encoding of novel associations. Here we test the hypothesis that a recently identified fast-expressing form of Hebbian synaptic plasticity (associative short-term potentiation) is a possible mechanism for WM encoding and maintenance. Our simulations using a spiking neural network model of cortex reproduce a range of cognitive memory effects in the classical multi-item WM task of encoding and immediate free recall of word lists. Memory reactivation in the model occurs in discrete oscillatory bursts rather than as sustained activity. We relate dynamic network activity as well as key synaptic characteristics to electrophysiological measurements. Our findings support the hypothesis that fast Hebbian short-term potentiation is a key WM mechanism.Key words: Hebbian plasticity; primacy; recency; short-term potentiation; word list learning; working memory
IntroductionWorking memory (WM) is a key component of cognition. It maintains information over seconds and minutes in a form that allows animals to act beyond the here and now. WM is updated by selectively attended external information and activated longterm memory representations. Mammalian prefrontal cortex (PFC) is generally believed to play a key role in WM (Fuster, 2009; D'Esposito and Postle, 2015).The most common theory about the neural mechanisms of WM is that of persistent elevated activity in a recurrently connected neural network, presumably located in the PFC (Funahashi et al., 1989; Goldman-Rakic, 1995; Tsakanikas and Relkin, 2007). This theory was implemented in early spiking neural network models of persistent activity WM (Camperi and Wang, 1998; Compte et al., 2000). However, recent reexamina-
Significance StatementWorking memory (WM) is a key component of cognition. Hypotheses about the neural mechanism behind WM are currently under revision. Reflecting recent findings of fast Hebbian synaptic plasticity in cortex, we test whether a cortical spiking neural network model with such a mechanism can learn a multi-item WM task (word list learning). We show that our model can reproduce human cognitive phenomena and achieve comparable memory performance in both free and cued recall while being simultaneously compatible with experimental data on structure, connectivity, and neurophysiology of the underlying cortical tissue. These findings are directly relevant to the ongoing paradigm shift in the WM field.The Journal of N...