How distributed is the brain-wide network that is recruited for cognition?

原始摘要

Half a century of neurophysiological recordings from single electrodes established a ‘localized’ viewpoint on function in the brain — that complex behaviour results from computations that are carried out and representations that occur across distinct brain areas, each of which has a specialized role. Data generated from new techniques for specific, high-throughput measurement of neuronal activity and behaviour in rodents have prompted an alternative viewpoint, which posits that neural encoding of behavioural variables is distributed across a wide range of areas: ‘everything, everywhere, all at once’. After briefly introducing these paradigms, we evaluate which of them better describes cognition — the manipulation of internal variables that enables flexible behaviour. Measurements of neuronal activity in both rodents and primates suggest that cognitive variables are reflected broadly but not ubiquitously across the brain, including, to a surprising degree, in regions engaged in controlling movement. We close by discussing why cognitive signals may appear in such areas, as well as the factors that affect the breadth of the brain-wide network that is recruited for cognition. Beevor, C. E. & Horsley, V. A. H. VI A minute analysis (experiments) of the various movements produced by stimulating in the monkey different regions of the cortical centre for the upper limb, as defined by Professor Ferrier. Philos. Trans. R. Soc. Lond. B 178 , 153–167 (1887). Maunsell, J. H. & Van Essen, D. C. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J. Neurophysiol. 49 , 1127–1147 (1983). Posani, L., Wang, S., Muscinelli, S. P., Paninski, L. & Fusi, S. Rarely categorical, always high-dimensional: how the neural code changes along the cortical hierarchy. Preprint at bioRxiv https://doi.org/10.1101/2024.11.15.623878 (2025). Johnston, W. J., Tetrick, S. M. & Freedman, D. J. The lateral intraparietal area preferentially supports stimulus selection in directed tasks compared to undirected free behavior. Preprint at bioRxiv https://doi.org/10.1101/2022.03.09.483625 (2022). Goodwin, S. J., Blackman, R. K., Sakellaridi, S. & Chafee, M. V. Executive control over cognition: stronger and earlier rule-based modulation of spatial category signals in prefrontal cortex relative to parietal cortex. J. Neurosci. 32 , 3499–3515 (2012). Nature Reviews Neuroscience thanks Anne Churchland, who co-reviewed with Gabriel Rojas-Bowe; Hendrikje Nienborg, who co-reviewed with Bharath Chandra Talluri; and the other anonymous reviewer(s) for their contribution to the peer review of this work. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.