Oscillations without cortex: Working memory modulates brainwaves in the endbrain of crows

Abstract

Complex cognition requires coordinated neuronal activity at the network level. In mammals, this coordination results in distinct dynamics of local field potentials (LFP) that have been central in many models of higher cognition. Because these models are based on mammalian data, they often implicitly assume a cortical organization. Higher associative regions of the brains of birds do not have cortical layering, yet these regions have neuronal single-cell correlates of higher cognition that are very similar to those found in mammals. Here we recorded LFP in the avian equivalent of prefrontal cortex while crows performed a highly controlled and cognitively demanding working memory task, adapted from monkeys. To further ensure that recordings reflected only cognitive processes detached from motor-related activities we trained and monitored the animals to keep their head still. We found signatures in local field potentials, modulated by working memory. Frequencies of a narrow gamma (30-59 Hz) and the beta band (13-19 Hz) contained information about the location of the target items on the screen and were modulated by working memory load. This indicates a critical involvement of these bands in ongoing cognitive processing. We also observed bursts in the beta and gamma frequencies, similar to those observed in monkeys. Such bursts are a vital part of activity silent models of working memory. Thus, despite the lack of a cortical organization the avian associative pallium can create LFP signatures reminiscent of those observed in primates. This points towards a critical cognitive function of oscillatory dynamics evolved through convergence in species capable of complex cognition. Relevance statementContemporary models of higher cognition, like those of working memory, often include temporal dynamics of neural activity such as gamma oscillations. Birds and mammals convergently evolved these cognitive functions and here we show that, despite the large evolutionary distance and largely different brain organization, crows share many of the oscillatory fingerprints reported in primates. This indicates that neural networks required for such LFP phenomena have evolved in parallel and may be critical to higher cognition.