Working memory capacity of crows and monkeys arises from similar neuronal computations

Abstract

Complex cognition relies on flexible working memory, which is severely limited in its capacity. The neuronal computations underlying these capacity limits have been extensively studied in humans and in monkeys, resulting in competing theoretical models. We probed the working memory capacity of crows (Corvus corone) in a change detection task, developed for monkeys (Macaca mulatta), while we performed extracellular recordings of the prefrontal-like area nidopallium caudolaterale. We found that neuronal encoding and maintenance of information were affected by item load, in a way that is virtually identical to results obtained from monkey prefrontal cortex. Contemporary neurophysiological models of working memory employ divisive normalization as an important mechanism that may result in the capacity limitation. As these models are usually conceptualized and tested in an exclusively mammalian context, it remains unclear if they fully capture a general concept of working memory or if they are restricted to the mammalian neocortex. Here we report that carrion crows and macaque monkeys share divisive normalization as a neuronal computation that is in line with mammalian models. This indicates that computational models of working memory developed in the mammalian cortex can also apply to non-cortical associative brain regions of birds.

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

“…For example, the capacity of WM, the number of individual items that can be maintained simultaneously, is comparable between crows and macaque monkeys (Balakhonov & Rose, 2017). Even single neuron correlates of WM in birds are virtually identical to those in mammals (Ditz & Nieder, 2016Moll & Nieder, 2015;Rinnert et al, 2019;Rose & Colombo, 2005) and we recently found that this also extends to the neurophysiological limits of WM capacity (Buschman et al, 2011;Hahn et al, 2021).…”

“…4C) that simultaneously promotes selective neuronal activity without runaway excitation due to divisive normalization (Fries, 2015;Lundqvist et al, 2010). Together with analysis from single-neuron activity in crows (Hahn et al, 2021), it suggests that crow gamma could have a similar role in selection and normalization despite being implemented on a different neural substrate.…”

“…The behavioral paradigm was executed by custom code written in Matlab using the Psychophysics (Brainard, 1997) and Biopsychology toolboxes (Rose et al, 2008). Further details about the experimental setup have been reported in (Hahn et al, 2021).…”

“…Data of single-cell neuronal activity for analysis of the spiking rate of the neuronal population (SFig. 5), was obtained from our previous study (Hahn et al, 2021).…”

Number neurons in the nidopallium of young domestic chicks

“…In birds, similar neurons have been described in the caudolateral nidopallium (NCL, Ditz and Nieder 2015). The NCL is believed to be an analogue of the PFC in the avian brain (Güntürkün et al 2021) and is involved in a variety of cognitive processes, including memory formation (Diekamp et al 2002, Hahn et al 2021, abstract rule learning (Veit and Nieder 2013), and action planning (Veit et al 2015).…”