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

被引:0
作者
Hahn, Lukas Alexander [1 ]
Balakhonov, Dmitry [1 ]
Fongaro, Erica [1 ]
Nieder, Andreas [2 ]
Rose, Jonas [1 ]
机构
[1] Ruhr Univ Bochum, Fac Psychol, Inst Cognit Neurosci, Neural Basis Learning, Bochum, Germany
[2] Univ Tubingen, Inst Neurobiol, Anim Physiol, Tubingen, Germany
来源
ELIFE | 2021年 / 10卷
关键词
Corvus corone; divisive normalization; working memory capacity; comparative cognition; Other; SHORT-TERM-MEMORY; INDIVIDUAL-DIFFERENCES; EXECUTIVE CONTROL; NORMALIZATION; MULTIPLE; CORTEX; INFORMATION; RESOURCES; LOCATIONS; PRECISION;
D O I
10.7554/eLife.72783; 10.7554/eLife.72783.sa0; 10.7554/eLife.72783.sa1; 10.7554/eLife.72783.sa2
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
eLife digest Working memory is the brain's ability to temporarily hold and manipulate information. It is essential for carrying out complex cognitive tasks, such as reasoning, planning, following instructions or solving problems. Unlike long-term memory, information is not stored and recalled, but held in an accessible state for brief periods. However, the capacity of working memory is very limited. Humans, for example, can only hold around four items of information simultaneously. There are various competing theories about how this limitation arises from the network of neurons in the brain. These models are based on studies of humans and other primates. But memory limitations are not exclusive to mammals. Indeed, the working memory of some birds, such as crows, has a similar capacity to humans despite the architecture of their brains being very different to mammals. So, how do brains with such distinct structural differences produce working memories with similar capacities? To investigate, Hahn et al. probed the working memory of carrion crows in a change detection task developed for macaque monkeys. Crows were trained to memorize varying numbers of colored squares and indicate which square had changed after a one second delay when the screen went blank. While the crows performed the task, Hahn et al. measured the activity of neurons in an area of the brain equivalent to the prefrontal cortex, the central hub of cognition in mammals. The experiments showed that neurons in the crow brain responded to the changing colors virtually the same way as neurons in monkeys. Hahn et al. also noticed that increasing the number of items the crows had to remember affected individual neurons in a similar fashion as had previously been observed in monkeys. This suggests that birds and monkeys share the same central mechanisms of, and limits to, working memory despite differences in brain architecture. The similarities across distantly related species also validates core ideas about the limits of working memory developed from studies of mammals. 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.
引用
收藏
页数:21
相关论文
共 66 条
  • [1] Independent resources for attentional tracking in the left and right visual hemifields
    Alvarez, GA
    Cavanagh, P
    [J]. PSYCHOLOGICAL SCIENCE, 2005, 16 (08) : 637 - 643
  • [2] Visual working memory represents a fixed number of items regardless of complexity
    Awh, Edward
    Barton, Brian
    Vogel, Edward K.
    [J]. PSYCHOLOGICAL SCIENCE, 2007, 18 (07) : 622 - 628
  • [3] Crows Rival Monkeys in Cognitive Capacity
    Balakhonov, Dmitry
    Rose, Jonas
    [J]. SCIENTIFIC REPORTS, 2017, 7
  • [4] Dynamic shifts of limited working memory resources in human vision
    Bays, Paul M.
    Husain, Masud
    [J]. SCIENCE, 2008, 321 (5890) : 851 - 854
  • [5] A Flexible Model of Working Memory
    Bouchacourt, Flora
    Buschman, Timothy J.
    [J]. NEURON, 2019, 103 (01) : 147 - +
  • [6] Post-encoding control of working memory enhances processing of relevant information in rhesus monkeys (Macaca mulatta)
    Brady, Ryan J.
    Hampton, Robert R.
    [J]. COGNITION, 2018, 175 : 26 - 35
  • [7] The psychophysics toolbox
    Brainard, DH
    [J]. SPATIAL VISION, 1997, 10 (04): : 433 - 436
  • [8] Neural substrates of cognitive capacity limitations
    Buschman, Timothy J.
    Siegel, Markus
    Roy, Jefferson E.
    Miller, Earl K.
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2011, 108 (27) : 11252 - 11255
  • [9] Carandini M, 1997, J NEUROSCI, V17, P8621
  • [10] Normalization as a canonical neural computation
    Carandini, Matteo
    Heeger, David J.
    [J]. NATURE REVIEWS NEUROSCIENCE, 2012, 13 (01) : 51 - 62