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 deep is the brain? The shallow brain hypothesis

Abstract

Deep learning and predictive coding architectures commonly assume that inference in neural networks is hierarchical. However, largely neglected in deep learning and predictive coding architectures is the neurobiological evidence that all hierarchical cortical areas, higher or lower, project to and receive signals directly from subcortical areas. Given these neuroanatomical facts, today’s dominance of cortico-centric, hierarchical architectures in deep learning and predictive coding networks is highly questionable; such architectures are likely to be missing essential computational principles the brain uses. In this Perspective, we present the shallow brain hypothesis: hierarchical cortical processing is integrated with a massively parallel process to which subcortical areas substantially contribute. This shallow architecture exploits the computational capacity of cortical microcircuits and thalamo-cortical loops that are not included in typical hierarchical deep learning and predictive coding networks. We argue that the shallow brain architecture provides several critical benefits over deep hierarchical structures and a more complete depiction of how mammalian brains achieve fast and flexible computational capabilities.

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

Access options

Buy this article

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

Fig. 1: Deep and shallow architectures.
Fig. 2: The shallow brain hypothesis.
Fig. 3: New computational potential in shallow architectures.

Similar content being viewed by others

References

  1. Hegde, J. & Felleman, D. J. Reappraising the functional implications of the primate visual anatomical hierarchy. Neuroscientist 13, 416–421 (2007).

    Article  PubMed  Google Scholar 

  2. LeCun, Y., Bengio, Y. & Hinton, G. Deep learning. Nature 521, 436–444 (2015).

    Article  CAS  PubMed  Google Scholar 

  3. Stokel-Walker, C. & Van Noorden, R. What ChatGPT and generative AI mean for science. Nature 614, 214–216 (2023).

    Article  CAS  PubMed  Google Scholar 

  4. He, K., Zhang, X., Ren, S. & Sun, J. Deep residual learning for image recognition. In 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR) 770–778 (2016).

  5. Russakovsky, O. et al. ImageNet large scale visual recognition challenge. Int. J. Comput. Vis. 115, 211–252 (2015).

    Article  Google Scholar 

  6. Xu, K. et al. Show, attend and tell: neural image caption generation with visual attention. In 32nd Int. Conf. on Machine Learning (eds F. Bach. & D. Blei) 2048–2057 (2015).

  7. Fukushima, K. Neocognitron—a self-organizing neural network model for a mechanism of pattern-recognition unaffected by shift in position. Biol. Cybern. 36, 193–202 (1980).

    Article  CAS  PubMed  Google Scholar 

  8. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol. 160, 106–154 (1962).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chang, L. & Tsao, D. Y. The code for facial identity in the primate brain. Cell 169, 1013–1028.e14 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yamins, D. L. et al. Performance-optimized hierarchical models predict neural responses in higher visual cortex. Proc. Natl Acad. Sci. USA 111, 8619–8624 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Guclu, U. & van Gerven, M. A. Deep neural networks reveal a gradient in the complexity of neural representations across the ventral stream. J. Neurosci. 35, 10005–10014 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Cichy, R. M., Khosla, A., Pantazis, D., Torralba, A. & Oliva, A. Comparison of deep neural networks to spatio-temporal cortical dynamics of human visual object recognition reveals hierarchical correspondence. Sci. Rep. 6, 27755 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Schrimpf, M. et al. The neural architecture of language: integrative modeling converges on predictive processing. Proc. Natl Acad. Sci. USA 118, e2015646118 (2021).

    Article  Google Scholar 

  14. Kriegeskorte, N. Deep neural networks: a new framework for modeling biological vision and brain information processing. Annu. Rev. Vis. Sci. 1, 417–446 (2015).

    Article  PubMed  Google Scholar 

  15. Yamins, D. L. & DiCarlo, J. J. Using goal-driven deep learning models to understand sensory cortex. Nat. Neurosci. 19, 356–365 (2016).

    Article  CAS  PubMed  Google Scholar 

  16. Friston, K. A theory of cortical responses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 815–836 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Rao, R. P. & Ballard, D. H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2, 79–87 (1999).

    Article  CAS  PubMed  Google Scholar 

  18. Lee, T. S. & Mumford, D. Hierarchical Bayesian inference in the visual cortex. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 20, 1434–1448 (2003).

    Article  PubMed  Google Scholar 

  19. Srinivasan, M. V., Laughlin, S. B. & Dubs, A. Predictive coding: a fresh view of inhibition in the retina. Proc. R. Soc. Lond. B Biol. Sci. 216, 427–459 (1982).

    Article  CAS  PubMed  Google Scholar 

  20. Dayan, P., Hinton, G. E., Neal, R. M. & Zemel, R. S. The Helmholtz machine. Neural Comput. 7, 889–904 (1995).

    Article  CAS  PubMed  Google Scholar 

  21. Dora, S., Bohte, S. M. & Pennartz, C. M. A. Deep gated Hebbian predictive coding accounts for emergence of complex neural response properties along the visual cortical hierarchy. Front. Comput. Neurosci. 15, 666131 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  22. McDermott, J. H., Wrobleski, D. & Oxenham, A. J. Recovering sound sources from embedded repetition. Proc. Natl Acad. Sci. USA 108, 1188–1193 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Mill, R. W., Bohm, T. M., Bendixen, A., Winkler, I. & Denham, S. L. Modelling the emergence and dynamics of perceptual organisation in auditory streaming. PLoS Comput. Biol. 9, e1002925 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kanai, R., Komura, Y., Shipp, S. & Friston, K. Cerebral hierarchies: predictive processing, precision and the pulvinar. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140169 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Schwartenbeck, P., FitzGerald, T. H., Mathys, C., Dolan, R. & Friston, K. The dopaminergic midbrain encodes the expected certainty about desired outcomes. Cereb. Cortex 25, 3434–3445 (2015).

    Article  PubMed  Google Scholar 

  26. Rikhye, R. V., Wimmer, R. D. & Halassa, M. M. Toward an integrative theory of thalamic function. Annu. Rev. Neurosci. 41, 163–183 (2018).

    Article  CAS  PubMed  Google Scholar 

  27. Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    Article  CAS  PubMed  Google Scholar 

  28. Minsky, M. & Papert, S. Perceptrons; An Introduction to Computational Geometry (MIT Press, 1969).

  29. 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 

  30. Tsao, D. Y., Schweers, N., Moeller, S. & Freiwald, W. A. Patches of face-selective cortex in the macaque frontal lobe. Nat. Neurosci. 11, 877–879 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hegde, J. & Van Essen, D. C. A comparative study of shape representation in macaque visual areas V2 and V4. Cereb. Cortex 17, 1100–1116 (2007).

    Article  PubMed  Google Scholar 

  32. Rockland, K. S. & Pandya, D. N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 179, 3–20 (1979).

    Article  CAS  PubMed  Google Scholar 

  33. Markov, N. T. et al. Cortical high-density counterstream architectures. Science 342, 1238406 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Markov, N. T. & Kennedy, H. The importance of being hierarchical. Curr. Opin. Neurobiol. 23, 187–194 (2013).

    Article  CAS  PubMed  Google Scholar 

  35. D’Souza, R. D. et al. Hierarchical and nonhierarchical features of the mouse visual cortical network. Nat. Commun. 13, 503 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Siegle, J. H. et al. Survey of spiking in the mouse visual system reveals functional hierarchy. Nature 592, 86–92 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Nakamura, H., Gattass, R., Desimone, R. & Ungerleider, L. G. The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques. J. Neurosci. 13, 3681–3691 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Burkhalter, A., D’Souza, R. D., Ji, W. & Meier, A. M. Integration of feedforward and feedback information streams in the modular architecture of mouse visual cortex. Annu. Rev. Neurosci. 46, 259–280 (2023).

    Article  PubMed  Google Scholar 

  39. Coogan, T. A. & Burkhalter, A. Hierarchical organization of areas in rat visual cortex. J. Neurosci. 13, 3749–3772 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Friston, K. The free-energy principle: a unified brain theory? Nat. Rev. Neurosci. 11, 127–138 (2010).

    Article  CAS  PubMed  Google Scholar 

  41. Bastos, A. M. et al. Canonical microcircuits for predictive coding. Neuron 76, 695–711 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Pennartz, C. M. A., Dora, S., Muckli, L. & Lorteije, J. A. M. Towards a unified view on pathways and functions of neural recurrent processing. Trends Neurosci. 42, 589–603 (2019).

    Article  CAS  PubMed  Google Scholar 

  43. Findling, C. et al. Brain-wide representations of prior information in mouse decision-making. Preprint at bioRxiv https://doi.org/10.1101/2023.07.04.547684 (2023).

  44. Keller, G. B. & Mrsic-Flogel, T. D. Predictive processing: a canonical cortical computation. Neuron 100, 424–435 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Keller, G. B., Bonhoeffer, T. & Hubener, M. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse. Neuron 74, 809–815 (2012).

    Article  CAS  PubMed  Google Scholar 

  46. Jordan, R. & Keller, G. B. Opposing influence of top-down and bottom-up input on excitatory layer 2/3 neurons in mouse primary visual cortex. Neuron 108, 1194–1206.e5 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Padamsey, Z. & Rochefort, N. L. Defying expectations: how neurons compute prediction errors in visual cortex. Neuron 108, 1016–1019 (2020).

    Article  CAS  PubMed  Google Scholar 

  48. Muzzu, T. & Saleem, A. B. Feature selectivity can explain mismatch signals in mouse visual cortex. Cell Rep. 37, 109772 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Walsh, K. S., McGovern, D. P., Clark, A. & O’Connell, R. G. Evaluating the neurophysiological evidence for predictive processing as a model of perception. Ann. N. Y. Acad. Sci. 1464, 242–268 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Schwiedrzik, C. M. & Freiwald, W. A. High-level prediction signals in a low-level area of the macaque face-processing hierarchy. Neuron 96, 89–97.e4 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Issa, E. B., Cadieu, C. F. & DiCarlo, J. J. Neural dynamics at successive stages of the ventral visual stream are consistent with hierarchical error signals. eLife 7, e42870 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Chao, Z. C., Takaura, K., Wang, L., Fujii, N. & Dehaene, S. Large-scale cortical networks for hierarchical prediction and prediction error in the primate brain. Neuron 100, 1252–1266.e3 (2018).

    Article  CAS  PubMed  Google Scholar 

  53. Spratling, M. W. A review of predictive coding algorithms. Brain Cogn. 112, 92–97 (2017).

    Article  CAS  PubMed  Google Scholar 

  54. Spratling, M. W. Fitting predictive coding to the neurophysiological data. Brain Res. 1720, 146313 (2019).

    Article  CAS  PubMed  Google Scholar 

  55. Bianchini, M. & Scarselli, F. On the complexity of neural network classifiers: a comparison between shallow and deep architectures. IEEE Trans. Neural Netw. Learn. Syst. 25, 1553–1565 (2014).

    Article  PubMed  Google Scholar 

  56. Cohen, N., Sharir, O. & Shashua, A. On the expressive power of deep learning: a tensor analysis. In 29th Annual Conference on Learning Theory (eds. Feldman, V., Rakhlin, A. & Shamir, O.) 698–728 (2016).

  57. Hinton, G. E. Training products of experts by minimizing contrastive divergence. Neural Comput. 14, 1771–1800 (2002).

    Article  PubMed  Google Scholar 

  58. Dabelow, L. & Ueda, M. Three learning stages and accuracy-efficiency tradeoff of restricted Boltzmann machines. Nat. Commun. 13, 5474 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Liao, R., Kornblith, S., Ren, M., Fleet, D. J. & Hinton, G. Gaussian–Bernoulli RBMs without tears. Preprint at arXiv https://doi.org/10.48550/ARXIV.2210.10318 (2022).

  60. Hilgetag, C. C. & Goulas, A. ‘Hierarchy’ in the organization of brain networks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375, 20190319 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).

    Article  CAS  PubMed  Google Scholar 

  62. Jones, E. G. The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 24, 595–601 (2001).

    Article  CAS  PubMed  Google Scholar 

  63. Sherman, S. M. & Guillery, R. W. Exploring the Thalamus and Its Role in Cortical Function 2nd edn (MIT Press, 2009).

  64. Halassa, M. Thalamus 1st edn (Cambridge Univ. Press, 2023).

  65. Kemp, J. M. & Powell, T. P. The cortico-striate projection in the monkey. Brain 93, 525–546 (1970).

    Article  CAS  PubMed  Google Scholar 

  66. Oka, H. Organization of the cortico-caudate projections. A horseradish peroxidase study in the cat. Exp. Brain Res. 40, 203–208 (1980).

    Article  CAS  PubMed  Google Scholar 

  67. Ito, S. & Feldheim, D. A. The mouse superior colliculus: an emerging model for studying circuit formation and function. Front. Neural Circuits 12, 10 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Basso, M. A. & May, P. J. Circuits for action and cognition: a view from the superior colliculus. Annu. Rev. Vis. Sci. 3, 197–226 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  69. May, P. J. The mammalian superior colliculus: laminar structure and connections. Prog. Brain Res. 151, 321–378 (2006).

    Article  PubMed  Google Scholar 

  70. McBride, E. G. et al. Influence of claustrum on cortex varies by area, layer, and cell type. Neuron 111, 275–290.e5 (2022).

    Article  PubMed  Google Scholar 

  71. Narikiyo, K. et al. The claustrum coordinates cortical slow-wave activity. Nat. Neurosci. 23, 741–753 (2020).

    Article  CAS  PubMed  Google Scholar 

  72. Jackson, J., Karnani, M. M., Zemelman, B. V., Burdakov, D. & Lee, A. K. Inhibitory control of prefrontal cortex by the claustrum. Neuron 99, 1029–1039.e4 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Legg, C. R., Mercier, B. & Glickstein, M. Corticopontine projection in the rat: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J. Comp. Neurol. 286, 427–441 (1989).

    Article  CAS  PubMed  Google Scholar 

  74. Habas, C. & Cabanis, E. A. Cortical projections to the human red nucleus: a diffusion tensor tractography study with a 1.5-T MRI machine. Neuroradiology 48, 755–762 (2006).

    Article  PubMed  Google Scholar 

  75. Tervo, D. G. et al. A designer AAV variant permits efficient retrograde access to projection neurons. Neuron 92, 372–382 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Murakami, T., Matsui, T., Uemura, M. & Ohki, K. Modular strategy for development of the hierarchical visual network in mice. Nature 608, 578–585 (2022).

    Article  CAS  PubMed  Google Scholar 

  77. Tang, L. & Higley, M. J. Layer 5 circuits in V1 differentially control visuomotor behavior. Neuron 105, 346–354.e5 (2020).

    Article  CAS  PubMed  Google Scholar 

  78. Takahashi, N. et al. Active dendritic currents gate descending cortical outputs in perception. Nat. Neurosci. 23, 1277–1285 (2020).

    Article  CAS  PubMed  Google Scholar 

  79. Fuster, J. M. The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe (Raven, 1980).

  80. 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 

  81. Oswald, M. J., Tantirigama, M. L., Sonntag, I., Hughes, S. M. & Empson, R. M. Diversity of layer 5 projection neurons in the mouse motor cortex. Front. Cell Neurosci. 7, 174 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Akintunde, A. & Buxton, D. F. Origins and collateralization of corticospinal, corticopontine, corticorubral and corticostriatal tracts: a multiple retrograde fluorescent tracing study. Brain Res. 586, 208–218 (1992).

    Article  CAS  PubMed  Google Scholar 

  83. Harris, K. D. & Shepherd, G. M. The neocortical circuit: themes and variations. Nat. Neurosci. 18, 170–181 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Musall, S. et al. Pyramidal cell types drive functionally distinct cortical activity patterns during decision-making. Nat. Neurosci. 26, 495–505 (2023).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Mohan, H. et al. Cortical glutamatergic projection neuron types contribute to distinct functional subnetworks. Nat. Neurosci. 26, 481–494 (2023).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Kuramoto, E. et al. Ventral medial nucleus neurons send thalamocortical afferents more widely and more preferentially to layer 1 than neurons of the ventral anterior–ventral lateral nuclear complex in the rat. Cereb. Cortex 25, 221–235 (2015).

    Article  PubMed  Google Scholar 

  87. Cruikshank, S. J. et al. Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32, 17813–17823 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Schroeder, A. et al. Inhibitory top-down projections from zona incerta mediate neocortical memory. Neuron 111, 727–738.e8 (2023).

    Article  CAS  PubMed  Google Scholar 

  89. Ahmadlou, M. et al. A cell type-specific cortico-subcortical brain circuit for investigatory and novelty-seeking behavior. Science 372, eabe9681 (2021).

    Article  CAS  PubMed  Google Scholar 

  90. Brenner, J. M., Beltramo, R., Gerfen, C. R., Ruediger, S. & Scanziani, M. A genetically defined tecto-thalamic pathway drives a system of superior-colliculus-dependent visual cortices. Neuron 111, 2247–2257.e7 (2023).

    Article  CAS  PubMed  Google Scholar 

  91. Guo, Z. V. et al. Maintenance of persistent activity in a frontal thalamocortical loop. Nature 545, 181–186 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Hsiao, K. et al. A thalamic orphan receptor drives variability in short-term memory. Cell 183, 522–536.e19 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Redinbaugh, M. J. et al. Thalamus modulates consciousness via layer-specific control of cortex. Neuron 106, 66–75.e12 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Aru, J., Suzuki, M. & Larkum, M. E. Cellular mechanisms of conscious processing. Trends Cogn. Sci. 24, 814–825 (2020).

    Article  PubMed  Google Scholar 

  95. Aru, J., Suzuki, M., Rutiku, R., Larkum, M. E. & Bachmann, T. Coupling the state and contents of consciousness. Front. Syst. Neurosci. 13, 43 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Suzuki, M. & Larkum, M. E. General anesthesia decouples cortical pyramidal neurons. Cell 180, 666–676.e13 (2020).

    Article  CAS  PubMed  Google Scholar 

  97. Schiff, N. D. et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600–603 (2007).

    Article  CAS  PubMed  Google Scholar 

  98. Bastos, A. M. et al. Neural effects of propofol-induced unconsciousness and its reversal using thalamic stimulation. eLife 10, e60824 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Crick, F. C. & Koch, C. What is the function of the claustrum. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 1271–1279 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Chevee, M., Finkel, E. A., Kim, S. J., O’Connor, D. H. & Brown, S. P. Neural activity in the mouse claustrum in a cross-modal sensory selection task. Neuron 110, 486–501.e7 (2022).

    Article  CAS  PubMed  Google Scholar 

  101. Huang, W., Qin, J., Zhang, C., Qin, H. & Xie, P. Footshock-induced activation of the claustrum–entorhinal cortical pathway in freely moving mice. Physiol. Res. 71, 695–701 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Smythies, J. On the function of object cells in the claustrum—key components in information processing in the visual system? Front. Cell Neurosci. 9, 443 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  103. Tsumoto, T. & Suda, K. Effects of stimulation of the dorsocaudal claustrum on activities of striate cortex neurons in the cat. Brain Res. 240, 345–349 (1982).

    Article  CAS  PubMed  Google Scholar 

  104. Remedios, R., Logothetis, N. K. & Kayser, C. A role of the claustrum in auditory scene analysis by reflecting sensory change. Front. Syst. Neurosci. 8, 44 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  105. Qadir, H. et al. The mouse claustrum synaptically connects cortical network motifs. Cell Rep. 41, 111860 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Taylor, N. L. et al. Structural connections between the noradrenergic and cholinergic system shape the dynamics of functional brain networks. Neuroimage 260, 119455 (2022).

    Article  CAS  PubMed  Google Scholar 

  107. Deutch, A. Y. & Roth, R. H. in Fundamental Neuroscience (eds M. J. Zigmond et al.) 193–234 (Academic, 1999).

  108. Chevalier, G. & Deniau, J. M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13, 277–280 (1990).

    Article  CAS  PubMed  Google Scholar 

  109. Voorn, P., Vanderschuren, L. J., Groenewegen, H. J., Robbins, T. W. & Pennartz, C. M. Putting a spin on the dorsal–ventral divide of the striatum. Trends Neurosci. 27, 468–474 (2004).

    Article  CAS  PubMed  Google Scholar 

  110. Budinger, E., Heil, P., Hess, A. & Scheich, H. Multisensory processing via early cortical stages: connections of the primary auditory cortical field with other sensory systems. Neuroscience 143, 1065–1083 (2006).

    Article  CAS  PubMed  Google Scholar 

  111. Benavidez, N. L. et al. Organization of the inputs and outputs of the mouse superior colliculus. Nat. Commun. 12, 4004 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Beltramo, R. & Scanziani, M. A collicular visual cortex: neocortical space for an ancient midbrain visual structure. Science 363, 64–69 (2019).

    Article  CAS  PubMed  Google Scholar 

  113. Constantinople, C. M. & Bruno, R. M. Effects and mechanisms of wakefulness on local cortical networks. Neuron 69, 1061–1068 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Aru, J., Siclari, F., Phillips, W. A. & Storm, J. F. Apical drive—a cellular mechanism of dreaming? Neurosci. Biobehav. Rev. 119, 440–455 (2020).

    Article  PubMed  Google Scholar 

  115. Wainstein, G., Muller, E. J., Taylor, N., Munn, B. & Shine, J. M. The role of the locus coeruleus in shaping adaptive cortical melodies. Trends Cogn. Sci. 26, 527–538 (2022).

    Article  PubMed  Google Scholar 

  116. Polack, P. O., Friedman, J. & Golshani, P. Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat. Neurosci. 16, 1331–1339 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Harris, K. D. & Thiele, A. Cortical state and attention. Nat. Rev. Neurosci. 12, 509–523 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Parikh, V., Kozak, R., Martinez, V. & Sarter, M. Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56, 141–154 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Puig, M. V. & Gulledge, A. T. Serotonin and prefrontal cortex function: neurons, networks, and circuits. Mol. Neurobiol. 44, 449–464 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Buhot, M. C., Martin, S. & Segu, L. Role of serotonin in memory impairment. Ann. Med. 32, 210–221 (2000).

    Article  CAS  PubMed  Google Scholar 

  121. Petroni, F., Panzeri, S., Hilgetag, C. C., Kotter, R. & Young, M. P. Simultaneity of responses in a hierarchical visual network. Neuroreport 12, 2753–2759 (2001).

    Article  CAS  PubMed  Google Scholar 

  122. Zeki, S. The rough seas of cortical cartography. Trends Neurosci. 41, 242–244 (2018).

    Article  CAS  PubMed  Google Scholar 

  123. Silvanto, J. Why is “blindsight” blind? A new perspective on primary visual cortex, recurrent activity and visual awareness. Conscious. Cogn. 32, 15–32 (2015).

    Article  PubMed  Google Scholar 

  124. Schmolesky, M. T. et al. Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272–3278 (1998).

    Article  CAS  PubMed  Google Scholar 

  125. Bullier, J. & Nowak, L. G. Parallel versus serial processing: new vistas on the distributed organization of the visual system. Curr. Opin. Neurobiol. 5, 497–503 (1995).

    Article  CAS  PubMed  Google Scholar 

  126. Douglas, R. J. & Martin, K. A. Mapping the matrix: the ways of neocortex. Neuron 56, 226–238 (2007).

    Article  CAS  PubMed  Google Scholar 

  127. Rockland, K. S. & Ichinohe, N. Some thoughts on cortical minicolumns. Exp. Brain Res. 158, 265–277 (2004).

    Article  PubMed  Google Scholar 

  128. Molnár, Z. & Rockland, K. S. in Neural Circuit and Cognitive Development Ch. 5 (eds J. Rubenstein, P. Rakic, B. Chen & K. Y. Kwan) 103–126 (Academic, 2020).

  129. Trojanowski, J. Q. & Jacobson, S. Medial pulvinar afferents to frontal eye fields in rhesus monkey demonstrated by horseradish peroxidase. Brain Res. 80, 395–411 (1974).

    Article  CAS  PubMed  Google Scholar 

  130. Baizer, J. S., Desimone, R. & Ungerleider, L. G. Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys. Vis. Neurosci. 10, 59–72 (1993).

    Article  CAS  PubMed  Google Scholar 

  131. Stanton, G. B., Goldberg, M. E. & Bruce, C. J. Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields. J. Comp. Neurol. 271, 473–492 (1988).

    Article  CAS  PubMed  Google Scholar 

  132. Lynch, J. C., Hoover, J. E. & Strick, P. L. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp. Brain Res. 100, 181–186 (1994).

    Article  CAS  PubMed  Google Scholar 

  133. Berman, R. A. & Wurtz, R. H. Exploring the pulvinar path to visual cortex. Prog. Brain Res. 171, 467–473 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Huerta, M. F., Krubitzer, L. A. & Kaas, J. H. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys: I. Subcortical connections. J. Comp. Neurol. 253, 415–439 (1986).

    Article  CAS  PubMed  Google Scholar 

  135. Leichnetz, G. R., Smith, D. J. & Spencer, R. F. Cortical projections to the paramedian tegmental and basilar pons in the monkey. J. Comp. Neurol. 228, 388–408 (1984).

    Article  CAS  PubMed  Google Scholar 

  136. Andersen, R. A., Asanuma, C., Essick, G. & Siegel, R. M. Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J. Comp. Neurol. 296, 65–113 (1990).

    Article  CAS  PubMed  Google Scholar 

  137. Lynch, J. C., Graybiel, A. M. & Lobeck, L. J. The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. J. Comp. Neurol. 235, 241–254 (1985).

    Article  CAS  PubMed  Google Scholar 

  138. Schall, J. D., Morel, A., King, D. J. & Bullier, J. Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J. Neurosci. 15, 4464–4487 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Vernet, M., Quentin, R., Chanes, L., Mitsumasu, A. & Valero-Cabre, A. Frontal eye field, where art thou? Anatomy, function, and non-invasive manipulation of frontal regions involved in eye movements and associated cognitive operations. Front. Integr. Neurosci. 8, 66 (2014).

    PubMed  PubMed Central  Google Scholar 

  140. Liu, Y., Yttri, E. A. & Snyder, L. H. Intention and attention: different functional roles for LIPd and LIPv. Nat. Neurosci. 13, 495–500 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Coe, B. C. & Munoz, D. P. Mechanisms of saccade suppression revealed in the anti-saccade task. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160192 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  142. Milardi, D. et al. Red nucleus connectivity as revealed by constrained spherical deconvolution tractography. Neurosci. Lett. 626, 68–73 (2016).

    Article  CAS  PubMed  Google Scholar 

  143. Na, J., Kakei, S. & Shinoda, Y. Cerebellar input to corticothalamic neurons in layers V and VI in the motor cortex. Neurosci. Res. 28, 77–91 (1997).

    Article  CAS  PubMed  Google Scholar 

  144. Martinez-Gonzalez, C., Bolam, J. P. & Mena-Segovia, J. Topographical organization of the pedunculopontine nucleus. Front. Neuroanat. 5, 22 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Sherman, S. M. & Guillery, R. W. Distinct functions for direct and transthalamic corticocortical connections. J. Neurophysiol. 106, 1068–1077 (2011).

    Article  PubMed  Google Scholar 

  146. de Kock, C. P., Bruno, R. M., Spors, H. & Sakmann, B. Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J. Physiol. 581, 139–154 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  147. Masamizu, Y. et al. Two distinct layer-specific dynamics of cortical ensembles during learning of a motor task. Nat. Neurosci. 17, 987–994 (2014).

    Article  CAS  PubMed  Google Scholar 

  148. Guo, K., Yamawaki, N., Svoboda, K. & Shepherd, G. M. G. Anterolateral motor cortex connects with a medial subdivision of ventromedial thalamus through cell type-specific circuits, forming an excitatory thalamo-cortico-thalamic loop via layer 1 apical tuft dendrites of layer 5b pyramidal tract type neurons. J. Neurosci. 38, 8787–8797 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Bharioke, A. et al. General anesthesia globally synchronizes activity selectively in layer 5 cortical pyramidal neurons. Neuron 110, 2024–2040.e10 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Larkum, M. A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex. Trends Neurosci. 36, 141–151 (2013).

    Article  CAS  PubMed  Google Scholar 

  151. Brea, J., Gaal, A. T., Urbanczik, R. & Senn, W. Prospective coding by spiking neurons. PLoS Comput. Biol. 12, e1005003 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  152. Roelfsema, P. R. & Holtmaat, A. Control of synaptic plasticity in deep cortical networks. Nat. Rev. Neurosci. 19, 166–180 (2018).

    Article  CAS  PubMed  Google Scholar 

  153. Lillicrap, T. P., Santoro, A., Marris, L., Akerman, C. J. & Hinton, G. Backpropagation and the brain. Nat. Rev. Neurosci. 21, 335–346 (2020).

    Article  CAS  PubMed  Google Scholar 

  154. Whittington, J. C. R. & Bogacz, R. Theories of error back-propagation in the brain. Trends Cogn. Sci. 23, 235–250 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  155. Xiong, Q., Znamenskiy, P. & Zador, A. M. Selective corticostriatal plasticity during acquisition of an auditory discrimination task. Nature 521, 348–351 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Cox, J. & Witten, I. B. Striatal circuits for reward learning and decision-making. Nat. Rev. Neurosci. 20, 482–494 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Park, J. M. et al. Deep and superficial layers of the primary somatosensory cortex are critical for whisker-based texture discrimination in mice. Preprint at bioRxiv https://doi.org/10.1101/2020.08.12.245381 (2022).

  158. Hong, Y. K., Lacefield, C. O., Rodgers, C. C. & Bruno, R. M. Sensation, movement and learning in the absence of barrel cortex. Nature 561, 542–546 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Von Neumann, J. The Computer and the Brain (Yale Univ. Press, 1958).

  160. Mo, C. & Sherman, S. M. A sensorimotor pathway via higher-order thalamus. J. Neurosci. 39, 692–704 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Lake, B. M., Ullman, T. D., Tenenbaum, J. B. & Gershman, S. J. Building machines that learn and think like people. Behav. Brain Sci. 40, e253 (2017).

    Article  PubMed  Google Scholar 

  162. Baroni, M. Linguistic generalization and compositionality in modern artificial neural networks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375, 20190307 (2020).

    Article  PubMed  Google Scholar 

  163. Ruediger, S. & Scanziani, M. Learning speed and detection sensitivity controlled by distinct cortico-fugal neurons in visual cortex. eLife 9, e59247 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Brooks, R. A. A robust layered control-system for a mobile robot. IEEE T Robotic Autom. 2, 14–23 (1986).

    Article  Google Scholar 

  165. Brooks, R. A. New approaches to robotics. Science 253, 1227–1232 (1991).

    Article  CAS  PubMed  Google Scholar 

  166. Haider, P., Ellenberger, B., Kriener, L., Jordan, J., Senn, W. & Petrovici, M. A. Latent equilibrium: a unified learning theory for arbitrarily fast computation with arbitrarily slow neurons. Adv. Neural Inf. Process. Syst. 34, 17839–17851 (2021).

    Google Scholar 

  167. Narayanan, R. T. et al. Beyond columnar organization: cell type- and target layer-specific principles of horizontal axon projection patterns in rat vibrissal cortex. Cereb. Cortex 25, 4450–4468 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  168. Chen, G., Scherr, F. & Maass, W. A data-based large-scale model for primary visual cortex enables brain-like robust and versatile visual processing. Sci. Adv. 8, eabq7592 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  169. Guest, J. M., Bast, A., Narayanan, R. T. & Oberlaender, M. Thalamus gates active dendritic computations in cortex during sensory processing. Preprint at bioRxiv https://doi.org/10.1101/2021.10.21.465325 (2021).

  170. Constantinople, C. M. & Bruno, R. M. Deep cortical layers are activated directly by thalamus. Science 340, 1591–1594 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Pluta, S. et al. A direct translaminar inhibitory circuit tunes cortical output. Nat. Neurosci. 18, 1631–1640 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Stuart, G., Spruston, N. & Häusser, M. Dendrites 3rd edn (Oxford Univ. Press, 2016).

  173. Major, G., Larkum, M. E. & Schiller, J. Active properties of neocortical pyramidal neuron dendrites. Annu. Rev. Neurosci. 36, 1–24 (2013).

    Article  CAS  PubMed  Google Scholar 

  174. Mikulasch, F. A., Rudelt, L., Wibral, M. & Priesemann, V. Where is the error? Hierarchical predictive coding through dendritic error computation. Trends Neurosci. 46, 45–59 (2022).

    Article  PubMed  Google Scholar 

  175. Richards, B. A. & Lillicrap, T. P. Dendritic solutions to the credit assignment problem. Curr. Opin. Neurobiol. 54, 28–36 (2019).

    Article  CAS  PubMed  Google Scholar 

  176. Guerguiev, J., Lillicrap, T. P. & Richards, B. A. Towards deep learning with segregated dendrites. eLife 6, e22901 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  177. Hawkins, J. & Ahmad, S. Why neurons have thousands of synapses, a theory of sequence memory in neocortex. Front. Neural Circuits 10, 23 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  178. Schiess, M., Urbanczik, R. & Senn, W. Somato-dendritic synaptic plasticity and error-backpropagation in active dendrites. PLoS Comput. Biol. 12, e1004638 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  179. Poirazi, P. & Papoutsi, A. Illuminating dendritic function with computational models. Nat. Rev. Neurosci. 21, 303–321 (2020).

    Article  CAS  PubMed  Google Scholar 

  180. Beniaguev, D., Segev, I. & London, M. Single cortical neurons as deep artificial neural networks. Neuron 109, 2727–2739.e3 (2021).

    Article  CAS  PubMed  Google Scholar 

  181. Cossell, L. et al. Functional organization of excitatory synaptic strength in primary visual cortex. Nature 518, 399–403 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Seeman, S. C. et al. Sparse recurrent excitatory connectivity in the microcircuit of the adult mouse and human cortex. eLife 7, e37349 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  183. Garner, A. R. & Keller, G. B. A cortical circuit for audio-visual predictions. Nat. Neurosci. 25, 98–105 (2022).

    Article  CAS  PubMed  Google Scholar 

  184. Ghazanfar, A. A. & Schroeder, C. E. Is neocortex essentially multisensory? Trends Cogn. Sci. 10, 278–285 (2006).

    Article  PubMed  Google Scholar 

  185. Fetsch, C. R., DeAngelis, G. C. & Angelaki, D. E. Bridging the gap between theories of sensory cue integration and the physiology of multisensory neurons. Nat. Rev. Neurosci. 14, 429–442 (2013).

    Article  CAS  PubMed  Google Scholar 

  186. Graybiel, A. M. The basal ganglia. Curr. Biol. 10, R509–R511 (2000).

    Article  CAS  PubMed  Google Scholar 

  187. Alexander, G. E., DeLong, M. R. & Strick, P. L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357–381 (1986).

    Article  CAS  PubMed  Google Scholar 

  188. Parent, A. et al. Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci. 23, S20–S27 (2000).

    Article  CAS  PubMed  Google Scholar 

  189. Takakusaki, K., Saitoh, K., Harada, H. & Kashiwayanagi, M. Role of basal ganglia–brainstem pathways in the control of motor behaviors. Neurosci. Res. 50, 137–151 (2004).

    Article  CAS  PubMed  Google Scholar 

  190. Graybiel, A. M., Aosaki, T., Flaherty, A. W. & Kimura, M. The basal ganglia and adaptive motor control. Science 265, 1826–1831 (1994).

    Article  CAS  PubMed  Google Scholar 

  191. Roseberry, T. K. et al. Cell-type-specific control of brainstem locomotor circuits by basal ganglia. Cell 164, 526–537 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Parent, M., Levesque, M. & Parent, A. Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J. Comp. Neurol. 439, 162–175 (2001).

    Article  CAS  PubMed  Google Scholar 

  193. Parent, M. & Parent, A. The pallidofugal motor fiber system in primates. Parkinsonism Relat. Disord. 10, 203–211 (2004).

    Article  PubMed  Google Scholar 

  194. Pennartz, C. M., Groenewegen, H. J. & Lopes da Silva, F. H. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog. Neurobiol. 42, 719–761 (1994).

    Article  CAS  PubMed  Google Scholar 

  195. Di Chiara, G., Porceddu, M. L., Morelli, M., Mulas, M. L. & Gessa, G. L. Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat. Brain Res. 176, 273–284 (1979).

    Article  PubMed  Google Scholar 

  196. Williams, L. E. & Holtmaat, A. Higher-order thalamocortical inputs gate synaptic long-term potentiation via disinhibition. Neuron 101, 91–102.e4 (2019).

    Article  CAS  PubMed  Google Scholar 

  197. Gambino, F. et al. Sensory-evoked LTP driven by dendritic plateau potentials in vivo. Nature 515, 116–119 (2014).

    Article  CAS  PubMed  Google Scholar 

  198. Anastasiades, P. G., Collins, D. P. & Carter, A. G. Mediodorsal and ventromedial thalamus engage distinct L1 circuits in the prefrontal cortex. Neuron 109, 314–330.e4 (2021).

    Article  CAS  PubMed  Google Scholar 

  199. Schmitt, L. I. et al. Thalamic amplification of cortical connectivity sustains attentional control. Nature 545, 219–223 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Inagaki, H. K. et al. A midbrain–thalamus–cortex circuit reorganizes cortical dynamics to initiate movement. Cell 185, 1065–1081.e23 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Wang, M. B. & Halassa, M. M. Thalamocortical contribution to flexible learning in neural systems. Netw. Neurosci. 6, 980–997 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  202. La Terra, D. et al. The role of higher-order thalamus during learning and correct performance in goal-directed behavior. eLife 11, e77177 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  203. Ruis, L., Andreas, J., Baroni, M., Bouchacourt, D. & Lake, B. M. A benchmark for systematic generalization in grounded language understanding. In Proc. 34th Int. Conf. Neural Information Processing Systems (eds. Larochelle, H. et al.) 19861–19872 (Curran, 2020).

  204. Lake, B. M. & Baroni, M. Generalization without systematicity: on the compositional skills of sequence-to-sequence recurrent networks. In Int. Conf. Machine Learning (eds. Dy, J. & Krause, A.) 2879–2888 (2018).

  205. Pfeiffer, J., Ruder, S., Vulić, I. & Ponti, E. M. Modular deep learning. Preprint at arXiv https://doi.org/10.48550/arXiv.2302.11529 (2023).

  206. Goyal, A. et al. Recurrent independent mechanisms. Preprint at arXiv https://doi.org/10.48550/arXiv.1909.10893 (2020).

  207. Albright, T. D., Jessell, T. M., Kandel, E. R. & Posner, M. I. Neural science: a century of progress and the mysteries that remain. Neuron 25, S1–S55 (2000).

    Article  PubMed  Google Scholar 

  208. 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 

  209. Verschure, P. F., Pennartz, C. M. & Pezzulo, G. The why, what, where, when and how of goal-directed choice: neuronal and computational principles. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130483 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  210. Dias, R., Robbins, T. W. & Roberts, A. C. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380, 69–72 (1996).

    Article  CAS  PubMed  Google Scholar 

  211. Wilson, R. C., Takahashi, Y. K., Schoenbaum, G. & Niv, Y. Orbitofrontal cortex as a cognitive map of task space. Neuron 81, 267–279 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  212. Fan, J., McCandliss, B. D., Fossella, J., Flombaum, J. I. & Posner, M. I. The activation of attentional networks. Neuroimage 26, 471–479 (2005).

    Article  PubMed  Google Scholar 

  213. Womelsdorf, T. & Everling, S. Long-range attention networks: circuit motifs underlying endogenously controlled stimulus selection. Trends Neurosci. 38, 682–700 (2015).

    Article  CAS  PubMed  Google Scholar 

  214. Cohen, M. R. & Maunsell, J. H. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 12, 1594–1600 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Reynolds, J. H. & Desimone, R. Interacting roles of attention and visual salience in V4. Neuron 37, 853–863 (2003).

    Article  CAS  PubMed  Google Scholar 

  216. Poort, J. et al. The role of attention in figure-ground segregation in areas V1 and V4 of the visual cortex. Neuron 75, 143–156 (2012).

    Article  CAS  PubMed  Google Scholar 

  217. Reep, R. L. & Corwin, J. V. Posterior parietal cortex as part of a neural network for directed attention in rats. Neurobiol. Learn. Mem. 91, 104–113 (2009).

    Article  PubMed  Google Scholar 

  218. Saalmann, Y. B., Pinsk, M. A., Wang, L., Li, X. & Kastner, S. The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337, 753–756 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  219. Rikhye, R. V., Gilra, A. & Halassa, M. M. Thalamic regulation of switching between cortical representations enables cognitive flexibility. Nat. Neurosci. 21, 1753–1763 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  220. Van der Werf, Y. D., Witter, M. P. & Groenewegen, H. J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev. 39, 107–140 (2002).

    Article  PubMed  Google Scholar 

  221. Groenewegen, H. J. & Berendse, H. W. The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei. Trends Neurosci. 17, 52–57 (1994).

    Article  CAS  PubMed  Google Scholar 

  222. Breton-Provencher, V., Drummond, G. T., Feng, J., Li, Y. & Sur, M. Spatiotemporal dynamics of noradrenaline during learned behaviour. Nature 606, 732–738 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Ren, J. et al. Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems. Cell 175, 472–487.e20 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. Lohani, S. et al. Spatiotemporally heterogeneous coordination of cholinergic and neocortical activity. Nat. Neurosci. 25, 1706–1713 (2022).

    Article  CAS  PubMed  Google Scholar 

  225. Morris, L. S. et al. Fronto-striatal organization: defining functional and microstructural substrates of behavioural flexibility. Cortex 74, 118–133 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  226. Apicella, P., Legallet, E., Nieoullon, A. & Trouche, E. Neglect of contralateral visual stimuli in monkeys with unilateral striatal dopamine depletion. Behav. Brain Res. 46, 187–195 (1991).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

M.S. discloses support for the research of this work from the Brain Science Foundation and the Sumitomo Foundation (2200084). C.M.A.P. discloses support for the research of this work from the European Union’s Horizon 2020 Framework Program for Research and Innovation (Human Brain Project SGA3, 945539). J.A. discloses support for the research of this work from the European Social Fund through the ‘ICT programme’ measure and the Estonian Research Council grant (PSG728).

Author information

Authors and Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding authors

Correspondence to Mototaka Suzuki or Jaan Aru.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Neuroscience thanks Andreas Burkhalter 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.

Glossary

Bayesian inference

A method of statistical analysis that is grounded in Bayes’ theorem, which describes how the probability of a hypothesis (posterior probability) is updated as new data (evidence) become available, given prior knowledge about the hypothesis (prior probability).

Cortico-cortical loops

Neural circuits that connect different regions of the cerebral cortex to one another, allowing communication and integration of information across various cortical areas. These loops can be either short range, connecting adjacent or nearby cortical regions, or long range, linking distant regions of the cortex.

Deep hierarchy

A hierarchical structure consisting of many layers (roughly analogous to cortical areas) through which information from the external world is processed step by step.

Deep learning architectures

Structured configurations of hierarchical, interconnected layers of artificial neurons, or nodes, in a neural network. Common types of deep learning architecture include feedforward convolutional neural networks and recurrent neural networks.

Hierarchical inference

The process of drawing conclusions from data wherein parameters are organized into different levels or layers. In hierarchical Bayesian inference, Bayesian statistics are employed within a layered framework, integrating prior knowledge at multiple levels to refine posterior distributions.

Higher-order thalamic nuclei

Thalamic nuclei can be categorized anatomically into first-order and higher-order nuclei. First-order nuclei receive driving afferents from ascending pathways, whereas the higher-order nuclei receive driving afferents from cortical layer 5 pyramidal (L5p) neurons. Notable examples of higher-order thalamic nuclei include the pulvinar and the medial dorsal nucleus.

Non-hierarchical lateral connections

Connections made between two cortical areas that are not distinguished hierarchically (for instance, primary auditory and visual cortex). This connectivity pattern is illustrated in Fig. 1b.

Recurrent connections

Connections in which the output of a neuron at a given layer is fed back as an input to either the same layer or a previous layer. This creates a loop in the network, allowing information, for instance, to persist and be reused across sequential steps.

Recurrent neural network

A class of neural networks in which connections between nodes form directed cycles, enabling the retention of information from previous inputs. This sequential memory feature makes recurrent neural networks suitable for tasks involving time-series or sequential data.

Reinforcement learning

A machine learning method in which an agent makes decisions and receives reinforcing feedback to train the network to improve its output (for example, reward for desired behaviours, punishment for behaviour resulting in undesirable output).

Shallow architectures

Architectures that do not consist of a deep hierarchy. Shallow architectures instead have a minimum number of layers.

Shallow processing

Computations carried out by a shallow architecture, namely in a few steps instead of tens or hundreds of layers of processing.

Thalamo-cortical loops

Bidirectional pathways between the thalamus and the cerebral cortex. Thalamo-cortical loops play a vital role in the regulation of consciousness, attention and sensory processing, and have been implicated in several neurological and psychiatric disorders.

Trans-thalamic connections

Connections made between two brain regions via the thalamus.

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

Suzuki, M., Pennartz, C.M.A. & Aru, J. How deep is the brain? The shallow brain hypothesis. Nat. Rev. Neurosci. 24, 778–791 (2023). https://doi.org/10.1038/s41583-023-00756-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41583-023-00756-z

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