Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

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

Abstract

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: A distributed view of functional neuroanatomy.
Fig. 2: ‘Deeply sampled’ tasks for studying the brain-wide basis of cognition by aggregating across many experiments.
Fig. 3: Uninstructed movements reflect working memory content during task performance.

Similar content being viewed by others

References

  1. Freedman, D. J. et al. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291, 312–316 (2001).

    Article  CAS  PubMed  Google Scholar 

  2. Seger, C. A. & Miller, E. K. Category learning in the brain. Annu. Rev. Neurosci. 33, 203–219 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Wallis, J. D., Anderson, K. C. & Miller, E. K. Single neurons in prefrontal cortex encode abstract rules. Nature 411, 953–956 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Stoet, G. & Snyder, L. H. Single neurons in posterior parietal cortex of monkeys encode cognitive set. Neuron 42, 1003–1012 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Mansouri, F. A., Freedman, D. J. & Buckley, M. J. Emergence of abstract rules in the primate brain. Nat. Rev. Neurosci. 21, 595–610 (2020).

    Article  CAS  PubMed  Google Scholar 

  6. Snyder, L. H., Batista, A. P. & Andersen, R. A. Coding of intention in the posterior parietal cortex. Nature 386, 167–170 (1997).

    Article  CAS  PubMed  Google Scholar 

  7. Cui, H. & Andersen, R. A. Posterior parietal cortex encodes autonomously selected motor plans. Neuron 56, 552–559 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Miller, E. K. & Cohen, J. D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  PubMed  Google Scholar 

  9. Christophel, T. B. et al. The distributed nature of working memory. Trends Cogn. Sci. 21, 111–124 (2017).

    Article  PubMed  Google Scholar 

  10. Haxby, J. V. et al. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425–2430 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. Spiridon, M. & Kanwisher, N. How distributed is visual category information in human occipito-temporal cortex? An fMRI study. Neuron 35, 1157–1165 (2002).

    Article  CAS  PubMed  Google Scholar 

  12. Op de Beeck, H. P., Haushofer, J. & Kanwisher, N. G. Interpreting fMRI data: maps, modules and dimensions. Nat. Rev. Neurosci. 9, 123–135 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fritsch, G. & Hitzig, E. Electric excitability of the cerebrum (Uber die elektrische Erregbarkeit des Grosshirns). Epilepsy Behav. 15, 123–130 (2009).

    Article  CAS  PubMed  Google Scholar 

  14. Ferrier, D. & Burdon-Sanderson, J. S. Experiments on the brain of monkeys. — no. I. Proc. R. Soc. Lond. 23, 409–430 (1874).

    Article  Google Scholar 

  15. 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).

    Article  Google Scholar 

  16. Penfield, W. & Boldrey, E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60, 389–443 (1937).

    Article  Google Scholar 

  17. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol. 160, 106–154.2 (1962).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hubel, D. H. & Wiesel, T. N. Ferrier lecture — functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B Biol. Sci. 198, 1–59 (1997).

    Google Scholar 

  19. Dubner, R. & Zeki, S. M. Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. Brain Res. 35, 528–532 (1971).

    Article  CAS  PubMed  Google Scholar 

  20. Zeki, S. M. Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J. Physiol. 236, 549–573 (1974).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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).

    Article  CAS  PubMed  Google Scholar 

  22. Gross, C. G., Bender, D. B. & Rocha-Miranda, C. E. Visual receptive fields of neurons in inferotemporal cortex of the monkey. Science 166, 1303–1306 (1969).

    Article  CAS  PubMed  Google Scholar 

  23. Gross, C. G., Rocha-Miranda, C. E. & Bender, D. B. Visual properties of neurons in inferotemporal cortex of the macaque. J. Neurophysiol. 35, 96–111 (1972).

    Article  CAS  PubMed  Google Scholar 

  24. Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tanji, J. & Evarts, E. V. Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J. Neurophysiol. 39, 1062–1068 (1976).

    Article  CAS  PubMed  Google Scholar 

  26. Georgopoulos, A. P., Kalaska, J. F., Caminiti, R. & Massey, J. T. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J. Neurosci. 2, 1527–1537 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bizzi, E. Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp. Brain Res. 6, 69–80 (1968).

    Article  CAS  PubMed  Google Scholar 

  28. Bizzi, E. & Schiller, P. H. Single unit activity in the frontal eye fields of unanesthetized monkeys during eye and head movement. Exp. Brain Res. 10, 150–158 (1970).

    Article  CAS  PubMed  Google Scholar 

  29. Wurtz, R. H. & Goldberg, M. E. Superior colliculus cell responses related to eye movements in awake monkeys. Science 171, 82–84 (1971).

    Article  CAS  PubMed  Google Scholar 

  30. Juavinett, A. L., Bekheet, G. & Churchland, A. K. Chronically implanted Neuropixels probes enable high-yield recordings in freely moving mice. eLife 8, e47188 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Luo, T. Z. et al. An approach for long-term, multi-probe Neuropixels recordings in unrestrained rats. eLife 9, e59716 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Steinmetz, N. A. et al. Neuropixels 2.0: a miniaturized high-density probe for stable, long-term brain recordings. Science 372, eabf4588 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Manley, J. et al. Simultaneous, cortex-wide dynamics of up to 1 million neurons reveal unbounded scaling of dimensionality with neuron number. Neuron 112, 1694–1709.e5 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sofroniew, N. J., Flickinger, D., King, J. & Svoboda, K. A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging. eLife 5, e14472 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Zong, W. et al. Large-scale two-photon calcium imaging in freely moving mice. Cell 185, 1240–1256.e30 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhang, Y. et al. Fast and sensitive GCaMP calcium indicators for imaging neural populations. Nature 615, 884–891 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Machado, T. A., Kauvar, I. V. & Deisseroth, K. Multiregion neuronal activity: the forest and the trees. Nat. Rev. Neurosci. 23, 683–704 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Mathis, A. et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289 (2018).

    Article  CAS  PubMed  Google Scholar 

  39. Pereira, T. D. et al. Fast animal pose estimation using deep neural networks. Nat. Methods 16, 117–125 (2019).

    Article  CAS  PubMed  Google Scholar 

  40. Pereira, T. D. et al. SLEAP: a deep learning system for multi-animal pose tracking. Nat. Methods 19, 486–495 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Stringer, C. et al. Spontaneous behaviors drive multidimensional, brainwide activity. Science 364, eaav7893 (2019).

    Article  CAS  Google Scholar 

  42. Musall, S., Kaufman, M. T., Juavinett, A. L., Gluf, S. & Churchland, A. K. Single-trial neural dynamics are dominated by richly varied movements. Nat. Neurosci. 22, 1677–1686 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Salkoff, D. B., Zagha, E., McCarthy, E. & McCormick, D. A. Movement and performance explain widespread cortical activity in a visual detection task. Cereb. Cortex 30, 421–437 (2020).

    Article  PubMed  Google Scholar 

  44. Allen, W. E. et al. Thirst regulates motivated behavior through modulation of brainwide neural population dynamics. Science 364, eaav3932 (2019).

    Article  CAS  Google Scholar 

  45. Flavell, S. W., Gogolla, N., Lovett-Barron, M. & Zelikowsky, M. The emergence and influence of internal states. Neuron 110, 2545–2570 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hayden, B. Y. The dangers of cortical brain maps. J. Cogn. Neurosci. 35, 372–375 (2023).

    Article  PubMed  Google Scholar 

  47. Steinmetz, N. A., Zatka-Haas, P., Carandini, M. & Harris, K. D. Distributed coding of choice, action and engagement across the mouse brain. Nature 576, 266–273 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. International Brain Laboratory et al. A brain-wide map of neural activity during complex behaviour. Nature 645, 177–191 (2025).

    Article  CAS  Google Scholar 

  49. Chen, S. et al. Brain-wide neural activity underlying memory-guided movement. Cell 187, 676–691.e16 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Khilkevich, A. et al. Brain-wide dynamics linking sensation to action during decision-making. Nature 634, 890–900 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. O’Shea, D. J. et al. The need for calcium imaging in nonhuman primates: new motor neuroscience and brain-machine interfaces. Exp. Neurol. 287, 437–451 (2017).

    Article  PubMed  Google Scholar 

  52. Bondy, A. G. et al. Coordinated cross-brain activity during accumulation of sensory evidence and decision commitment. Preprint at bioRxiv https://doi.org/10.1101/2024.08.21.609044 (2024).

  53. Zagha, E. et al. The importance of accounting for movement when relating neuronal activity to sensory and cognitive processes. J. Neurosci. 42, 1375–1382 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 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).

  55. Van Essen, D. C. et al. Cerebral cortical folding, parcellation, and connectivity in humans, nonhuman primates, and mice. Proc. Natl Acad. Sci. USA 116, 26173–26180 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Gămănuţ, R. et al. The mouse cortical connectome, characterized by an ultra-dense cortical graph, maintains specificity by distinct connectivity profiles. Neuron 97, 698–715.e10 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Markov, N. T. et al. A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb. Cortex 24, 17–36 (2014).

    Article  CAS  PubMed  Google Scholar 

  58. Theodoni, P. et al. Structural attributes and principles of the neocortical connectome in the marmoset monkey. Cereb. Cortex 32, 15–28 (2022).

    Article  Google Scholar 

  59. Magrou, L. et al. The meso-connectomes of mouse, marmoset, and macaque: network organization and the emergence of higher cognition. Cereb. Cortex 34, bhae174 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Newsome, W. T., Britten, K. H. & Movshon, J. A. Neuronal correlates of a perceptual decision. Nature 341, 52–54 (1989).

    Article  CAS  PubMed  Google Scholar 

  61. Shadlen, M. N. & Newsome, W. T. Motion perception: seeing and deciding. Proc. Natl Acad. Sci. USA 93, 628–633 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kim, J.-N. & Shadlen, M. N. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat. Neurosci. 2, 176–185 (1999).

    Article  PubMed  Google Scholar 

  63. Horwitz, G. D. & Newsome, W. T. Separate signals for target selection and movement specification in the superior colliculus. Science 284, 1158–1161 (1999).

    Article  CAS  PubMed  Google Scholar 

  64. Roitman, J. D. & Shadlen, M. N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22, 9475–9489 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Shadlen, M. N., Kiani, R., Hanks, T. D. & Churchland, A. K. in Better than Conscious? Decision Making, the Human Mind, and Implications for Institutions 71–101 (MIT Press, 2008).

  66. Ding, L. & Gold, J. I. Caudate encodes multiple computations for perceptual decisions. J. Neurosci. 30, 15747–15759 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Stine, G. M., Trautmann, E. M., Jeurissen, D. & Shadlen, M. N. A neural mechanism for terminating decisions. Neuron 111, 2601–2613.e5 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Branam, K., Gold, J. I. & Ding, L. The subthalamic nucleus contributes causally to perceptual decision-making in monkeys. eLife 13, RP98345 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Steinemann, N. et al. Direct observation of the neural computations underlying a single decision. eLife 12, RP90859 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Britten, K. H., Newsome, W. T., Shadlen, M. N., Celebrini, S. & Movshon, J. A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996).

    Article  CAS  PubMed  Google Scholar 

  71. Celebrini, S. & Newsome, W. T. Microstimulation of extrastriate area MST influences performance on a direction discrimination task. J. Neurophysiol. 73, 437–448 (1995).

    Article  CAS  PubMed  Google Scholar 

  72. Jun, E. J. et al. Causal role for the primate superior colliculus in the computation of evidence for perceptual decisions. Nat. Neurosci. 24, 1121–1131 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hernández, A., Salinas, E., Garcı́a, R. & Romo, R. Discrimination in the sense of flutter: new psychophysical measurements in monkeys. J. Neurosci. 17, 6391–6400 (1997).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Romo, R., Brody, C. D., Hernández, A. & Lemus, L. Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399, 470–473 (1999).

    Article  CAS  PubMed  Google Scholar 

  75. Hernández, A., Zainos, A. & Romo, R. Neuronal correlates of sensory discrimination in the somatosensory cortex. Proc. Natl Acad. Sci. USA 97, 6191–6196 (2000).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Salinas, E., Hernández, A., Zainos, A. & Romo, R. Periodicity and firing rate as candidate neural codes for the frequency of vibrotactile stimuli. J. Neurosci. 20, 5503–5515 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Hernández, A., Zainos, A. & Romo, R. Temporal evolution of a decision-making process in medial premotor cortex. Neuron 33, 959–972 (2002).

    Article  PubMed  Google Scholar 

  78. Romo, R., Hernández, A., Zainos, A., Lemus, L. & Brody, C. D. Neuronal correlates of decision-making in secondary somatosensory cortex. Nat. Neurosci. 5, 1217–1225 (2002).

    Article  CAS  PubMed  Google Scholar 

  79. Brody, C. D., Hernández, A., Zainos, A. & Romo, R. Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cereb. Cortex 13, 1196–1207 (2003).

    Article  PubMed  Google Scholar 

  80. Romo, R., Hernández, A. & Zainos, A. Neuronal correlates of a perceptual decision in ventral premotor cortex. Neuron 41, 165–173 (2004).

    Article  CAS  PubMed  Google Scholar 

  81. Hernández, A. et al. Decoding a perceptual decision process across cortex. Neuron 66, 300–314 (2010).

    Article  PubMed  Google Scholar 

  82. Fassihi, A., Akrami, A., Esmaeili, V. & Diamond, M. E. Tactile perception and working memory in rats and humans. Proc. Natl Acad. Sci. USA 111, 2331–2336 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Fassihi, A., Akrami, A., Pulecchi, F., Schönfelder, V. & Diamond, M. E. Transformation of perception from sensory to motor cortex. Curr. Biol. 27, 1585–1596.e6 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Akrami, A., Kopec, C. D., Diamond, M. E. & Brody, C. D. Posterior parietal cortex represents sensory history and mediates its effects on behaviour. Nature 554, 368–372 (2018).

    Article  CAS  PubMed  Google Scholar 

  85. Esmaeili, V. & Diamond, M. E. Neuronal correlates of tactile working memory in prefrontal and vibrissal somatosensory cortex. Cell Rep. 27, 3167–3181.e5 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Freedman, D. J. & Assad, J. A. Experience-dependent representation of visual categories in parietal cortex. Nature 443, 85–88 (2006).

    Article  CAS  PubMed  Google Scholar 

  87. Fitzgerald, J. K., Freedman, D. J. & Assad, J. A. Generalized associative representations in parietal cortex. Nat. Neurosci. 14, 1075–1079 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Swaminathan, S. K. & Freedman, D. J. Preferential encoding of visual categories in parietal cortex compared with prefrontal cortex. Nat. Neurosci. 15, 315–320 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Swaminathan, S. K., Masse, N. Y. & Freedman, D. J. A comparison of lateral and medial intraparietal areas during a visual categorization task. J. Neurosci. 33, 13157–13170 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Rishel, C. A., Huang, G. & Freedman, D. J. Independent category and spatial encoding in parietal cortex. Neuron 77, 969–979 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Sarma, A., Masse, N. Y., Wang, X.-J. & Freedman, D. J. Task-specific versus generalized mnemonic representations in parietal and prefrontal cortices. Nat. Neurosci. 19, 143–149 (2016).

    Article  CAS  PubMed  Google Scholar 

  92. Mohan, K., Zhu, O. & Freedman, D. J. Interaction between neuronal encoding and population dynamics during categorization task switching in parietal cortex. Neuron 109, 700–712.e4 (2021).

    Article  CAS  PubMed  Google Scholar 

  93. Zhou, Y., Mohan, K. & Freedman, D. J. Abstract encoding of categorical decisions in medial superior temporal and lateral intraparietal cortices. J. Neurosci. 42, 9069–9081 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Peysakhovich, B. et al. Primate superior colliculus is causally engaged in abstract higher-order cognition. Nat. Neurosci. https://doi.org/10.1038/s41593-024-01744-x (2024).

  95. Zhou, Y., Zhu, O. & Freedman, D. J. Posterior parietal cortex plays a causal role in abstract memory-based visual categorical decisions. J. Neurosci. 43, 4315–4328 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Thura, D. & Cisek, P. Deliberation and commitment in the premotor and primary motor cortex during dynamic decision making. Neuron 81, 1401–1416 (2014).

    Article  CAS  PubMed  Google Scholar 

  97. Kaufman, M. T., Churchland, M. M., Ryu, S. I. & Shenoy, K. V. Vacillation, indecision and hesitation in moment-by-moment decoding of monkey motor cortex. eLife 4, e04677 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Mione, V., Brunamonti, E., Pani, P., Genovesio, A. & Ferraina, S. Dorsal premotor cortex neurons signal the level of choice difficulty during logical decisions. Cell Rep. 32, 107961 (2020).

    Article  CAS  PubMed  Google Scholar 

  99. Diaz-deLeon, G. et al. An abstract categorical decision code in dorsal premotor cortex. Proc. Natl Acad. Sci. USA 119, e2214562119 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Maisson, D. J.-N. et al. Widespread coding of navigational variables in prefrontal cortex. Curr. Biol. 33, 3478–3488.e3 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Ferrera, V. P., Yanike, M. & Cassanello, C. Frontal eye field neurons signal changes in decision criteria. Nat. Neurosci. 12, 1458–1462 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Mante, V., Sussillo, D., Shenoy, K. V. & Newsome, W. T. Context-dependent computation by recurrent dynamics in prefrontal cortex. Nature 503, 78–84 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Siegel, M., Buschman, T. J. & Miller, E. K. Cortical information flow during flexible sensorimotor decisions. Science 348, 1352–1355 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Charlton, J. A. & Goris, R. L. T. Abstract deliberation by visuomotor neurons in prefrontal cortex. Nat. Neurosci. 27, 1167–1175 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ding, L. & Gold, J. I. Separate, causal roles of the caudate in saccadic choice and execution in a perceptual decision task. Neuron 75, 865–874 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Doi, T., Fan, Y., Gold, J. I. & Ding, L. The caudate nucleus contributes causally to decisions that balance reward and uncertain visual information. eLife 9, e56694 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Noel, J.-P. et al. Coding of latent variables in sensory, parietal, and frontal cortices during closed-loop virtual navigation. eLife 11, e80280 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Kaufman, M. T., Churchland, M. M., Ryu, S. I. & Shenoy, K. V. Cortical activity in the null space: permitting preparation without movement. Nat. Neurosci. 17, 440–448 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Hasnain, M. A. et al. Separating cognitive and motor processes in the behaving mouse. Nat. Neurosci. 28, 640–653 (2025).

    Article  CAS  PubMed  Google Scholar 

  110. Rosen, M. C. & Freedman, D. J. Multiplexing of cognitive encoding by oculomotor networks leads to incidental gaze shifts. Proc. Natl Acad. Sci. USA 122, e2422331122 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Erlich, J. C., Bialek, M. & Brody, C. D. A cortical substrate for memory-guided orienting in the rat. Neuron 72, 330–343 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Mangin, E. N., Chen, J., Lin, J. & Li, N. Behavioral measurements of motor readiness in mice. Curr. Biol. 33, 3610–3624.e4 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Cazettes, F. et al. Facial expressions in mice reveal latent cognitive variables and their neural correlates. Nat. Neurosci. https://doi.org/10.1038/s41593-025-02071-5 (2025).

  114. Yin, C. et al. Spontaneous movements and their relationship to neural activity fluctuate with latent engagement states. Neuron 113, 3048–3063.e5 (2025).

    Article  CAS  PubMed  Google Scholar 

  115. Dotson, N. M., Hoffman, S. J., Goodell, B. & Gray, C. M. Feature-based visual short-term memory is widely distributed and hierarchically organized. Neuron 99, 215–226.e4 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Lakshminarasimhan, K. J. et al. Tracking the mind’s eye: primate gaze behavior during virtual visuomotor navigation reflects belief dynamics. Neuron 106, 662–674.e5 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Stavropoulos, A., Lakshminarasimhan, K. J. & Angelaki, D. E. Belief embodiment through eye movements facilitates memory-guided navigation. Nat. Commun. https://doi.org/10.1038/s41467-025-66080-5 (2025).

  118. Caron, A. & Ester, E. F. Human gaze behaviors track stimulus meaning. Preprint at bioRxiv https://doi.org/10.1101/2025.08.08.669367 (2025).

  119. van Ede, F., Chekroud, S. R. & Nobre, A. C. Human gaze tracks attentional focusing in memorized visual space. Nat. Hum. Behav. 3, 462–470 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  120. Linde-Domingo, J. & Spitzer, B. Geometry of visuospatial working memory information in miniature gaze patterns. Nat. Hum. Behav. 8, 336–348 (2024).

    Article  PubMed  Google Scholar 

  121. Zokaei, N., Board, A. G., Manohar, S. G. & Nobre, A. C. Modulation of the pupillary response by the content of visual working memory. Proc. Natl Acad. Sci. USA 116, 22802–22810 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Prut, Y. & Fetz, E. E. Primate spinal interneurons show pre-movement instructed delay activity. Nature 401, 590–594 (1999).

    Article  CAS  PubMed  Google Scholar 

  123. Tremblay, S., Testard, C., DiTullio, R. W., Inchauspé, J. & Petrides, M. Neural cognitive signals during spontaneous movements in the macaque. Nat. Neurosci. 26, 295–305 (2023).

    Article  CAS  PubMed  Google Scholar 

  124. Yang, S., Dong, Y. & Kiyonaga, A. Flexible working memory in the peripheral nervous system. Preprint at bioRxiv https://doi.org/10.1101/2025.09.26.678884 (2025).

  125. Guo, Z. V. et al. Flow of cortical activity underlying a tactile decision in mice. Neuron 81, 179–194 (2014).

    Article  CAS  PubMed  Google Scholar 

  126. Komiyama, T. et al. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464, 1182–1186 (2010).

    Article  CAS  PubMed  Google Scholar 

  127. Zatka-Haas, P., Steinmetz, N. A., Carandini, M. & Harris, K. D. Sensory coding and the causal impact of mouse cortex in a visual decision. eLife 10, e63163 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Pinto, L. et al. Task-dependent changes in the large-scale dynamics and necessity of cortical regions. Neuron 104, 810–824.e9 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Arlt, C. et al. Cognitive experience alters cortical involvement in goal-directed navigation. eLife 11, e76051 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. 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).

  131. McKee, J. L., Riesenhuber, M., Miller, E. K. & Freedman, D. J. Task dependence of visual and category representations in prefrontal and inferior temporal cortices. J. Neurosci. 34, 16065–16075 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Kar, K., Kubilius, J., Schmidt, K., Issa, E. B. & DiCarlo, J. J. Evidence that recurrent circuits are critical to the ventral stream’s execution of core object recognition behavior. Nat. Neurosci. 22, 974–983 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Latimer, K. W. & Freedman, D. J. Low-dimensional encoding of decisions in parietal cortex reflects long-term training history. Nat. Commun. 14, 1010 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Chowdhury, S. A. & DeAngelis, G. C. Fine discrimination training alters the causal contribution of macaque area MT to depth perception. Neuron 60, 367–377 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Liu, L. D. & Pack, C. C. The contribution of area MT to visual motion perception depends on training. Neuron 95, 436–446.e3 (2017).

    Article  CAS  PubMed  Google Scholar 

  136. Zerbi, V. et al. Rapid reconfiguration of the functional connectome after chemogenetic locus coeruleus activation. Neuron 103, 702–718.e5 (2019).

    Article  CAS  PubMed  Google Scholar 

  137. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Crowe, D. A. et al. Prefrontal neurons transmit signals to parietal neurons that reflect executive control of cognition. Nat. Neurosci. 16, 1484–1491 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Kawai, R. et al. Motor cortex is required for learning but not for executing a motor skill. Neuron 86, 800–812 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Mizes, K. G. C., Lindsey, J., Escola, G. S. & Ölveczky, B. P. The role of motor cortex in motor sequence execution depends on demands for flexibility. Nat. Neurosci. 27, 2466–2475 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. International Brain Laboratory et al. Reproducibility of in vivo electrophysiological measurements in mice. eLife 13, RP100840 (2025).

    Article  PubMed Central  Google Scholar 

  142. Kriegeskorte, N. & Kievit, R. A. Representational geometry: integrating cognition, computation, and the brain. Trends Cogn. Sci. 17, 401–412 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  143. Bernardi, S. et al. The geometry of abstraction in the hippocampus and prefrontal cortex. Cell 183, 954–967.e21 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Kriegeskorte, N. & Wei, X.-X. Neural tuning and representational geometry. Nat. Rev. Neurosci. 22, 703–718 (2021).

    Article  CAS  PubMed  Google Scholar 

  145. Trautmann, E. M. et al. Large-scale high-density brain-wide neural recording in nonhuman primates. Nat. Neurosci. 28, 1562–1575 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Trepka, E. B., Zhu, S., Xia, R., Chen, X. & Moore, T. Functional interactions among neurons within single columns of macaque V1. eLife 11, e79322 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Shi, Y. et al. Rapid, concerted switching of the neural code in inferotemporal cortex. Preprint at bioRxiv https://doi.org/10.1101/2023.12.06.570341 (2023).

  148. Panichello, M. F. et al. Intermittent rate coding and cue-specific ensembles support working memory. Nature 636, 422–429 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Chung, J. E. et al. High-density single-unit human cortical recordings using the Neuropixels probe. Neuron 110, 2409–2421.e3 (2022).

    Article  CAS  PubMed  Google Scholar 

  150. Khanna, A. R. et al. Single-neuronal elements of speech production in humans. Nature 626, 603–610 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Leonard, M. K. et al. Large-scale single-neuron speech sound encoding across the depth of human cortex. Nature 626, 593–602 (2024).

    Article  CAS  PubMed  Google Scholar 

  152. Michaels, J. A. et al. Sensory expectations shape neural population dynamics in motor circuits. Nature https://doi.org/10.1038/s41586-025-09690-9 (2025).

  153. Namima, T., Kempkes, E., Zamarashkina, P., Owen, N. & Pasupathy, A. High-density recording reveals sparse clusters (but not columns) for shape and texture encoding in macaque V4. J. Neurosci. 45, e1893232024 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Liu, Y. et al. A high-density 1,024-channel probe for brain-wide recordings in non-human primates. Nat. Neurosci. 27, 1620–1631 (2024).

    Article  CAS  PubMed  Google Scholar 

  155. Clark, A. M. et al. An optrode array for spatiotemporally-precise large-scale optogenetic stimulation of deep cortical layers in non-human primates. Commun. Biol. 7, 329 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Sadakane, O. et al. Long-term two-photon calcium imaging of neuronal populations with subcellular resolution in adult non-human primates. Cell Rep. 13, 1989–1999 (2015).

    Article  CAS  PubMed  Google Scholar 

  157. Miller, C. T. et al. Marmosets: a neuroscientific model of human social behavior. Neuron 90, 219–233 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Mitchell, J. F. & Leopold, D. A. The marmoset monkey as a model for visual neuroscience. Neurosci. Res. 93, 20–46 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  159. Findling, C. et al. Brain-wide representations of prior information in mouse decision-making. Nature 645, 192–200 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Burgess, C. P. et al. High-yield methods for accurate two-alternative visual psychophysics in head-fixed mice. Cell Rep. 20, 2513–2524 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Abbott, L. F. et al. An international laboratory for systems and computational neuroscience. Neuron 96, 1213–1218 (2017).

    Article  CAS  Google Scholar 

  162. International Brain Laboratory et al. Standardized and reproducible measurement of decision-making in mice. eLife 10, e63711 (2021).

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge funding support from the Margot and Tom Pritzker Foundation, the NSF-Simons National Institute for Theory and Mathematics in Biology, NIH R01EY019041 and NIH R01EY037119.

Author information

Authors and Affiliations

Authors

Contributions

M.C.R. researched data for the article. Both authors provided substantial contributions to the discussion of its content, wrote the article, and reviewed and edited the manuscript before submission.

Corresponding authors

Correspondence to Matthew C. Rosen or David J. Freedman.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

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.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosen, M.C., Freedman, D.J. How distributed is the brain-wide network that is recruited for cognition?. Nat. Rev. Neurosci. 27, 138–150 (2026). https://doi.org/10.1038/s41583-025-00992-5

Download citation

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41583-025-00992-5

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing