Abstract
This chapter discusses how many features of cortical anatomy and physiology can be understood in the light of a predictive coding theory of brain function. In Sect. 7.1, we briefly discuss the theoretical reasons to suppose that the brain is likely to use predictive coding. One key theoretical underpinning of predictive coding is the free energy principle, which argues that brains must maximize the evidence for their (generative) model of sensory inputs: a process of ‘active inference’. In Sect. 7.2, we discuss how active inference predicts commonalities in the extrinsic connections of sensory and motor systems. Such commonalities are found in their hierarchical structure (shown by laminar characteristics), their topography, their pharmacology and physiology. In Sect. 7.3, we show how the equations describing hierarchical message passing within a predictive coding scheme can be mapped on to key features of intrinsic connections, namely the canonical cortical microcircuit, and their implications for the oscillatory dynamics of different cell populations. In Sect. 7.4, we briefly review some empirical evidence for predictive coding in the brain.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adams RA, Shipp S, Friston KJ (2013) Predictions not commands: active inference in the motor system. Brain Struct Funct 218:611–643. doi:10.1007/s00429-012-0475-5
Alink A, Schwiedrzik CM, Kohler A et al (2010) Stimulus predictability reduces responses in primary visual cortex. J Neurosci 30:2960–2966. doi:10.1523/JNEUROSCI.3730-10.2010
Anderson JC, Martin KAC (2006) Synaptic connection from cortical area V4 to V2 in macaque monkey. J Comp Neurol 495:709–721. doi:10.1002/cne.20914
Angelucci A, Bullier J (2003) Reaching beyond the classical receptive field of V1 neurons: horizontal or feedback axons? J Physiol Paris 97:141–154. doi:10.1016/j.jphysparis.2003.09.001
Barceló F, Suwazono S, Knight RT (2000) Prefrontal modulation of visual processing in humans. Nat Neurosci 3:399–403. doi:10.1038/73975
Bastos AM, Usrey WM, Adams RA et al (2012) Canonical microcircuits for predictive coding. Neuron 76:695–711. doi:10.1016/j.neuron.2012.10.038
Bendixen A, Schröger E, Winkler I (2009) I heard that coming: event-related potential evidence for stimulus-driven prediction in the auditory system. J Neurosci 29:8447–8451. doi:10.1523/JNEUROSCI.1493-09.2009
Bendixen A, SanMiguel I, Schröger E (2012) Early electrophysiological indicators for predictive processing in audition: a review. Int J Psychophysiol 83:120–131. doi:10.1016/j.ijpsycho.2011.08.003
Berkes P, Orbán G, Lengyel M, Fiser J (2011) Spontaneous cortical activity reveals hallmarks of an optimal internal model of the environment. Science 331:83–87. doi:10.1126/science.1195870
Binshtok AM, Fleidervish IA, Sprengel R, Gutnick MJ (2006) NMDA receptors in layer 4 spiny stellate cells of the mouse barrel cortex contain the NR2C subunit. J Neurosci 26:708–715. doi:10.1523/JNEUROSCI.4409-05.2006
Bullier J, Kennedy H, Salinger W (1984) Branching and laminar origin of projections between visual cortical areas in the cat. J Comp Neurol 228:329–341. doi:10.1002/cne.902280304
Bullier J, Hupé JM, James A, Girard P (1996) Functional interactions between areas V1 and V2 in the monkey. J Physiol Paris 90:217–220
Chu Z, Galarreta M, Hestrin S (2003) Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 23:96–102
Constantinople CM, Bruno RM (2013) Deep cortical layers are activated directly by thalamus. Science 340:1591–1594. doi:10.1126/science.1236425
Covic EN, Sherman SM (2011) Synaptic properties of connections between the primary and secondary auditory cortices in mice. Cereb Cortex 21:2425–2441. doi:10.1093/cercor/bhr029
Dancause N, Barbay S, Frost SB et al (2006) Ipsilateral connections of the ventral premotor cortex in a new world primate. J Comp Neurol 495:374–390. doi:10.1002/cne.20875
De Pasquale R, Sherman SM (2011) Synaptic properties of corticocortical connections between the primary and secondary visual cortical areas in the mouse. J Neurosci 31:16494–16506. doi:10.1523/JNEUROSCI.3664-11.2011
Desimone R (1996) Neural mechanisms for visual memory and their role in attention. Proc Natl Acad Sci U S A 93:13494–13499
Douglas RJ, Martin KA (1991) A functional microcircuit for cat visual cortex. J Physiol 440:735–769
Douglas RJ, Martin KAC, Whitteridge D (1989) A canonical microcircuit for neocortex. Neural Comput 1:480–488. doi:10.1162/neco.1989.1.4.480
Durstewitz D (2009) Implications of synaptic biophysics for recurrent network dynamics and active memory. Neural Netw 22:1189–1200. doi:10.1016/j.neunet.2009.07.016
Engbert R, Mergenthaler K, Sinn P, Pikovsky A (2011) An integrated model of fixational eye movements and microsaccades. Proc Natl Acad Sci U S A 108:E765–E770. doi:10.1073/pnas.1102730108
Esterman M, Yantis S (2010) Perceptual expectation evokes category-selective cortical activity. Cereb Cortex 20:1245–1253. doi:10.1093/cercor/bhp188
Feldman H, Friston KJ (2010) Attention, uncertainty, and free-energy. Front Hum Neurosci 4:215. doi:10.3389/fnhum.2010.00215
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47
Ferrer JM, Kato N, Price DJ (1992) Organization of association projections from area 17 to areas 18 and 19 and to suprasylvian areas in the cat’s visual cortex. J Comp Neurol 316:261–278. doi:10.1002/cne.903160302
Fox K, Sato H, Daw N (1990) The effect of varying stimulus intensity on NMDA-receptor activity in cat visual cortex. J Neurophysiol 64:1413–1428
Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563. doi:10.1126/science.291.5508.1560
Friston K (2005) A theory of cortical responses. Philos Trans R Soc Lond B Biol Sci 360:815–836. doi:10.1098/rstb.2005.1622
Friston K (2008) Hierarchical models in the brain. PLoS Comput Biol 4:e1000211. doi:10.1371/journal.pcbi.1000211
Friston K (2010) The free-energy principle: a unified brain theory? Nat Rev Neurosci 11:127–138. doi:10.1038/nrn2787
Friston K, Kiebel S (2009) Cortical circuits for perceptual inference. Neural Netw 22:1093–1104. doi:10.1016/j.neunet.2009.07.023
Friston KJ, Daunizeau J, Kilner J, Kiebel SJ (2010) Action and behavior: a free-energy formulation. Biol Cybern 102:227–260. doi:10.1007/s00422-010-0364-z
Friston K, Adams RA, Perrinet L, Breakspear M (2012) Perceptions as hypotheses: saccades as experiments. Front Psychol 3:151. doi:10.3389/fpsyg.2012.00151
Garrido MI, Kilner JM, Kiebel SJ, Friston KJ (2007) Evoked brain responses are generated by feedback loops. Proc Natl Acad Sci U S A 104:20961–20966. doi:10.1073/pnas.0706274105
Garrido MI, Kilner JM, Stephan KE, Friston KJ (2009) The mismatch negativity: a review of underlying mechanisms. Clin Neurophysiol 120:453–463. doi:10.1016/j.clinph.2008.11.029
Ghosh S, Porter R (1988) Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. J Physiol 400:617–629
Ghosh S, Brinkman C, Porter R (1987) A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis). J Comp Neurol 259:424–444. doi:10.1002/cne.902590309
Haeusler S, Maass W (2007) A statistical analysis of information-processing properties of lamina-specific cortical microcircuit models. Cereb Cortex 17:149–162. doi:10.1093/cercor/bhj132
Harrison SA, Tong F (2009) Decoding reveals the contents of visual working memory in early visual areas. Nature 458:632–635. doi:10.1038/nature07832
Harrison LM, Stephan KE, Rees G, Friston KJ (2007) Extra-classical receptive field effects measured in striate cortex with fMRI. NeuroImage 34:1199–1208. doi:10.1016/j.neuroimage.2006.10.017
Hatanaka N, Nambu A, Yamashita A et al (2001) Somatotopic arrangement and corticocortical inputs of the hindlimb region of the primary motor cortex in the macaque monkey. Neurosci Res 40:9–22
Hatanaka N, Tokuno H, Hamada I et al (2003) Thalamocortical and intracortical connections of monkey cingulate motor areas. J Comp Neurol 462:121–138. doi:10.1002/cne.10720
Hopfinger JB, Buonocore MH, Mangun GR (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3:284–291. doi:10.1038/72999
Hupé JM, James AC, Payne BR et al (1998) Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature 394:784–787. doi:10.1038/29537
Janata P (2001) Brain electrical activity evoked by mental formation of auditory expectations and images. Brain Topogr 13:169–193
Kätzel D, Zemelman BV, Buetfering C et al (2011) The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nat Neurosci 14:100–107. doi:10.1038/nn.2687
Knight RT (1984) Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol 59:9–20
Knight RT, Scabini D, Woods DL (1989) Prefrontal cortex gating of auditory transmission in humans. Brain Res 504:338–342
Kosslyn SM, Thompson WL (2003) When is early visual cortex activated during visual mental imagery? Psychol Bull 129:723–746. doi:10.1037/0033-2909.129.5.723
Kraemer DJM, Macrae CN, Green AE, Kelley WM (2005) Musical imagery: sound of silence activates auditory cortex. Nature 434:158. doi:10.1038/434158a
Larkum ME, Senn W, Lüscher H-R (2004) Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb Cortex 14:1059–1070. doi:10.1093/cercor/bhh065
Lefort S, Tomm C, Floyd Sarria J-C, Petersen CCH (2009) The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61:301–316. doi:10.1016/j.neuron.2008.12.020
Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114–140. doi:10.1002/cne.903380109
Maier A, Adams GK, Aura C, Leopold DA (2010) Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation. Front Syst Neurosci. doi:10.3389/fnsys.2010.00031
Matelli M, Camarda R, Glickstein M, Rizzolatti G (1986) Afferent and efferent projections of the inferior area 6 in the macaque monkey. J Comp Neurol 251:281–298. doi:10.1002/cne.902510302
Mechelli A, Price CJ, Friston KJ, Ishai A (2004) Where bottom-up meets top-down: neuronal interactions during perception and imagery. Cereb Cortex 14:1256–1265. doi:10.1093/cercor/bhh087
Meyer T, Olson CR (2011) Statistical learning of visual transitions in monkey inferotemporal cortex. Proc Natl Acad Sci U S A 108:19401–19406. doi:10.1073/pnas.1112895108
Meyer HS, Schwarz D, Wimmer VC et al (2011) Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. Proc Natl Acad Sci 108:16807–16812. doi:10.1073/pnas.1113648108
Muckli L, Kohler A, Kriegeskorte N, Singer W (2005) Primary visual cortex activity along the apparent-motion trace reflects illusory perception. PLoS Biol 3:e265. doi:10.1371/journal.pbio.0030265
Mumford D (1992) On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Biol Cybern 66:241–251
Muñoz A, Woods TM, Jones EG (1999) Laminar and cellular distribution of AMPA, kainate, and NMDA receptor subunits in monkey sensory-motor cortex. J Comp Neurol 407:472–490
Murray SO, Kersten D, Olshausen BA et al (2002) Shape perception reduces activity in human primary visual cortex. Proc Natl Acad Sci U S A 99:15164–15169. doi:10.1073/pnas.192579399
Nemoto I (2012) Evoked magnetoencephalographic responses to omission of a tone in a musical scale. J Acoust Soc Am 131:4770–4784. doi:10.1121/1.4714916
Nordby H, Hammerborg D, Roth WT, Hugdahl K (1994) ERPs for infrequent omissions and inclusions of stimulus elements. Psychophysiology 31:544–552
Olsen SR, Bortone DS, Adesnik H, Scanziani M (2012) Gain control by layer six in cortical circuits of vision. Nature 483:47–52. doi:10.1038/nature10835
Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1–26
Raij T, McEvoy L, Mäkelä JP, Hari R (1997) Human auditory cortex is activated by omissions of auditory stimuli. Brain Res 745:134–143
Rao RP, Ballard DH (1999) Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2:79–87. doi:10.1038/4580
Rockland KS, Drash GW (1996) Collateralized divergent feedback connections that target multiple cortical areas. J Comp Neurol 373:529–548. doi:10.1002/(SICI)1096-9861(19960930)373:4<529::AID-CNE5>3.0.CO;2–3
Roopun AK, Middleton SJ, Cunningham MO et al (2006) A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortex. Proc Natl Acad Sci U S A 103:15646–15650. doi:10.1073/pnas.0607443103
Roopun AK, Kramer MA, Carracedo LM et al (2008) Period concatenation underlies interactions between gamma and beta rhythms in neocortex. Front Cell Neurosci 2:1. doi:10.3389/neuro.03.001.2008
Salin PA, Bullier J (1995) Corticocortical connections in the visual system: structure and function. Physiol Rev 75:107–154
Schmidlin E, Brochier T, Maier MA et al (2008) Pronounced reduction of digit motor responses evoked from macaque ventral premotor cortex after reversible inactivation of the primary motor cortex hand area. J Neurosci 28:5772–5783. doi:10.1523/JNEUROSCI.0944-08.2008
Self MW, Kooijmans RN, Supèr H et al (2012) Different glutamate receptors convey feedforward and recurrent processing in macaque V1. Proc Natl Acad Sci U S A 109:11031–11036. doi:10.1073/pnas.1119527109
Shima K, Tanji J (1998) Involvement of NMDA and non-NMDA receptors in the neuronal responses of the primary motor cortex to input from the supplementary motor area and somatosensory cortex: studies of task-performing monkeys. Jpn J Physiol 48:275–290
Shimazu H, Maier MA, Cerri G et al (2004) Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. J Neurosci 24:1200–1211. doi:10.1523/JNEUROSCI.4731-03.2004
Shipp S (2005) The importance of being agranular: a comparative account of visual and motor cortex. Philos Trans R Soc Lond B Biol Sci 360:797–814. doi:10.1098/rstb.2005.1630
Shipp S (2007) Structure and function of the cerebral cortex. Curr Biol 17:R443–R449. doi:10.1016/j.cub.2007.03.044
Shipp S, Zeki S (1989a) The organization of connections between areas V5 and V1 in macaque monkey visual cortex. Eur J Neurosci 1:309–332
Shipp S, Zeki S (1989b) The organization of connections between areas V5 and V2 in macaque monkey visual cortex. Eur J Neurosci 1:333–354
Shlosberg D, Amitai Y, Azouz R (2006) Time-dependent, layer-specific modulation of sensory responses mediated by neocortical layer 1. J Neurophysiol 96:3170–3182. doi:10.1152/jn.00520.2006
Spratling MW (2010) Predictive coding as a model of response properties in cortical area V1. J Neurosci 30:3531–3543. doi:10.1523/JNEUROSCI.4911-09.2010
Spratling MW (2012) Predictive coding as a model of the V1 saliency map hypothesis. Neural Netw 26:7–28. doi:10.1016/j.neunet.2011.10.002
Summerfield C, Trittschuh EH, Monti JM et al (2008) Neural repetition suppression reflects fulfilled perceptual expectations. Nat Neurosci 11:1004–1006. doi:10.1038/nn.2163
Thomson AM, Bannister AP (2003) Interlaminar connections in the neocortex. Cereb Cortex 13:5–14. doi:10.1093/cercor/13.1.5
Thomson AM, West DC, Wang Y, AP B (2002) Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2–5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb Cortex 12:936–953
Todorovic A, van Ede F, Maris E, de Lange FP (2011) Prior expectation mediates neural adaptation to repeated sounds in the auditory cortex: an MEG study. J Neurosci 31:9118–9123. doi:10.1523/JNEUROSCI.1425-11.2011
Tokuno H, Tanji J (1993) Input organization of distal and proximal forelimb areas in the monkey primary motor cortex: a retrograde double labeling study. J Comp Neurol 333:199–209. doi:10.1002/cne.903330206
Traynelis SF, Wollmuth LP, McBain CJ et al (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405–496. doi:10.1124/pr.109.002451
Usrey WM, Fitzpatrick D (1996) Specificity in the axonal connections of layer VI neurons in tree shrew striate cortex: evidence for distinct granular and supragranular systems. J Neurosci 16:1203
von Helmholtz H (1866) Handbuch der physiologischen Optik: mit 213 in den Text eingedruckten Holzschnitten und 11 Tafeln. Voss
Wacongne C, Labyt E, van Wassenhove V et al (2011) Evidence for a hierarchy of predictions and prediction errors in human cortex. Proc Natl Acad Sci U S A 108:20754–20759. doi:10.1073/pnas.1117807108
Weiler N, Wood L, Yu J et al (2008) Top-down laminar organization of the excitatory network in motor cortex. Nat Neurosci 11:360–366. doi:10.1038/nn2049
Wozny C, Williams SR (2011) Specificity of synaptic connectivity between layer 1 inhibitory interneurons and layer 2/3 pyramidal neurons in the rat neocortex. Cereb Cortex 21:1818–1826. doi:10.1093/cercor/bhq257
Wyart V, Nobre AC, Summerfield C (2012) Dissociable prior influences of signal probability and relevance on visual contrast sensitivity. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1120118109
Yabe H, Tervaniemi M, Reinikainen K, Näätänen R (1997) Temporal window of integration revealed by MMN to sound omission. Neuroreport 8:1971–1974
Yamaguchi S, Knight RT (1990) Gating of somatosensory input by human prefrontal cortex. Brain Res 521:281–288
Zagha E, Casale AE, Sachdev RNS et al (2013) Motor cortex feedback influences sensory processing by modulating network state. Neuron 79:567–578. doi:10.1016/j.neuron.2013.06.008
Zeki S, Shipp S (1988) The functional logic of cortical connections. Nature 335:311–317. doi:10.1038/335311a0
Zilles K, Schlaug G, Matelli M et al (1995) Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. J Anat 187(Pt 3):515–537
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Adams, R.A., Friston, K.J., Bastos, A.M. (2015). Active Inference, Predictive Coding and Cortical Architecture. In: Casanova, M., Opris, I. (eds) Recent Advances on the Modular Organization of the Cortex. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9900-3_7
Download citation
DOI: https://doi.org/10.1007/978-94-017-9900-3_7
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-017-9899-0
Online ISBN: 978-94-017-9900-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)