Abstract
During the perception-to-action cycle, our cerebral cortex mediates the interactions between the environment and the perceptual-executive systems of the brain. At the top of the executive hierarchy, prefrontal cortical microcircuits are assumed to bind perceptual and executive control information to guide goal-driven behavior. Here, we discuss new results that show the involvement of prefrontal cortical inter-laminar microcircuits in the executive control of behavior. Recent results show that during perception and executive selection phases, cell firing in the localized prefrontal layers and caudate-putamen region exhibited a similar location preference on spatial-trials, but less on object- trials. When the perceptual-executive microcircuit became facilitated by electrically micro-stimulating the prefrontal infra-granular-cell layers with signal patterns previously derived from neuron firing in the supra-granular-layers, it was shown to produce stimulation-induced spatial preference (similar to neural tuning) in the percent correct performance only during spatial trials. These results suggested that inter-laminar prefrontal microcircuits play causal roles to the executive control of behavior across the perception-to-action cycle.
Keywords
- Cortical microcircuits
- Executive control
- Minicolumn
- Prefrontal cortex
- Primates
- MIMO model
- Causal relationship
- Perception-to-action
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Alexander GE, DeLong ME, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381
Alivisatos AP, Andrews AM, Boyden ES, Chun M, Church GM, Deisseroth K, Donoghue JP, Fraser SE, Lippincott-Schwartz J, Looger LL, Masmanidis S, McEuen PL, Nurmikko AV, Park H, Peterka DS, Reid C, Roukes ML, Scherer A, Schnitzer M, Sejnowski TJ, Shepard KL, Tsao D, Turrigiano G, Weiss PS, Xu C, Yuste R, Zhuang X (2013) Nanotools for neuroscience and brain activity mapping. ACS Nano 7:1850–1866
Atencio CA, Schreiner CE (2010) Columnar connectivity and laminar processing in cat primary auditory cortex. PLoS One 5(3), e9521
Jones EG (2000) Microcolumns in the cerebral cortex. A historical overview of the concept of micro- or minicolumns. Proc Natl Acad Sci U S A 97(10):5019–5021
Barbas H, Hilgetag CC, Saha S, Dermon CR, Suski JL (2005) Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey. BMC Neurosci 6:32
Bastos AM et al (2012) Canonical microcircuits for predictive coding. Neuron 76:695–711
Berger TW et al (2011) A cortical neural prosthesis for restoring and enhancing memory. J Neural Eng 8(4):046017
Botvinick M, Nystrom LE, Fissell K, Carter CS, Cohen JD (1999) Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402(6758):179–181
Brennan AR, Arnsten AF (2008) Neuronal mechanisms underlying attention deficit hyperactivity disorder: the influence of arousal on prefrontal cortical function. Ann N Y Acad Sci 1129:236–245
Buffalo EA, Fries P, Landmanc R, Buschman TJ, Desimone R (2011) Laminar differences in gamma and alpha coherence in the ventral stream. Proc Natl Acad Sci U S A 108:11262–11267
Bugbee NM, Goldman-Rakic PS (1983) Columnar organization of corticocortical projections in squirrel and rhesus monkeys: similarity of column width in species differing in cortical volume. J Comp Neurol 220:355–364
Buschman TJ, Denovellis EL, Diogo C, Bullock D, Miller EK (2012) Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76(4):838–846
Buxhoeveden DP, Casanova MF (2002) The minicolumn hypothesis in neuroscience. Brain 125(5):935–951
Buxhoeveden D, Fobbs A, Roy E, Casanova MF (2002) Quantitative comparison of radial cell columns in children with Down syndrome and controls. J Intellect Disabil Res 46(1):76–81
Casanova MF (2005) An apologia for a paradigm shift in neurosciences. In: Casanova MF (ed) Neocortical modularity and the cell minicolumn. Nova Biomedical Publishers, New York, pp 33–55
Casanova MF (2007) Schizophrenia seen as a deficit in the modulation of cortical minicolumns by monoaminergic systems. Int Rev Psychiatry 19(4):361–372
Casanova MF (2008) The significance of minicolumnar size variability in autism: a perspective from comparative anatomy (ch. 16). In: Zimmerman A (ed) Autism current theories and evidence. Current clinical neurology. The Humana Press, Totowa, pp 349–360
Casanova MF (2012) The minicolunopathy of autism. In: Buxbaum JD, Hof PR (eds) The neuroscience of autism spectrum disorder. Academic, Amsterdam, pp 327–334
Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002a) Minicolumnar pathology in autism. Neurology 58:428–432
Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002b) Neuronal density and architecture (gray level index) in the brains of autistic patients. J Child Neurol 17(7):515–521
Casanova MF, Buxhoeveden D, Gomez J (2003a) Disruption in the inhibitory architecture of the cell minicolumn: implications for autism. Neuroscientist 9(6):496–507
Casanova MF, Buxhoeveden D, Switala A, Roy E (2003b) Rett syndrome as a minicolumnopathy. Clin Neuropathol 22:163–168
Casanova MF, van Kooten I, Switala AE, van Engeland H, Heinsen H, Steinbusch HWM, Hof PR, Trippe J, Stone J, Schmitz C (2006a) Minicolumnar abnormalities in autism. Acta Neuropathol 112(3):287–303
Casanova MF, van Kooten I, Switala AE, van Engeland H, Heinsen H, Steinbusch HWM, Hof PR, Schmitz C (2006b) Abnormalities of cortical minicolumnar organization in the prefrontal lobes of autistic patients. Clin Neurosci Res 6(3):127–133
Casanova MF, Trippe JT II, Switala AE (2007) A temporal continuity to the vertical organization of the human neocortex. Cereb Cortex 17(1):130–137
Casanova MF et al (2008) Neuronal distribution in the neocortex of schizophrenic patients. Psychiatry Res 158(3):267–277
Casanova MF, El-Baz A, Vanbogaert E, Narahari P, Switala A (2010) A topographic study of minicolumnar core width by lamina comparison between autistic subjects and controls: possible minicolumnar disruption due to an anatomical element in-common to multiple laminae. Brain Pathol 20:451–458
Casanova MF, El-Baz A, Switala AE (2011) Laws of conservation as related to brain growth, aging, and evolution: symmetry of the minicolumn. Front Neuroanat 5:66
Casanova MF, Baruth JM, El-Baz A, Tasman A, Sears L, Sokhadze EM (2012) Repetitive TMS (rTMS) modulates ERP indices of attention in autism. Transl Neurosci 3(2):170–180
Casanova MF, El-Baz A, Kamat SS, Dombroski BA, Khalifa F, Elnakib A, Soliman A, Allison-McNutt A, Andrew AE (2013) Focal cortical dysplasias in autism spectrum disorders. Acta Neuropathol Commun 1:67. doi:10.1186/2051-5960-1-67
Chance SA, Casanova MF, Switala AE, Crow TJ, Esiri MM (2006) Minicolumn thinning in temporal lobe association cortex but not primary auditory cortex in normal human ageing. Acta Neuropathol 111(5):459–464
Chance SA, Casanova MF, Switala AE, Crow TJ (2008) Auditory cortex asymmetry, altered minicolumn spacing and absence of ageing effects in schizophrenia. Brain 131:3178–3192
Chance SA, Clover L, Cousijn H, Currah L, Pettingill R, Esiri MM (2011) Microanatomical correlates of cognitive ability and decline: normal ageing, MCI, and Alzheimer’s disease. Cereb Cortex 21(8):1870–1878
Constantinople CM, Bruno RM (2013) Deep cortical layers are activated directly from thalamus. Science 340(6140):1591–1594
Das A, Gilbert CD (1995) Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex. Nature 375(6534):780–784
DeFelipe J, Markram H, Rockland KS (2012) The neocortical column. Front Neuroanat 6:22
Di Rosa E, Crow TJ, Walker MA, Black G, Chance SA (2009) Reduced neuron density, enlarged minicolumn spacing and altered ageing effects in fusiform cortex in schizophrenia. Psychiatry Res 166(2–3):102–115
Dobbs D (2010) Schizophrenia: the making of a troubled mind. Nature 468:154–156
Duncan J, Johnson R, Swales M, Freer C (1997) Frontal lobe deficits after head injury: unity and diversity of function. Cognit Neuropsychol 14:713–741
Du J, Blanche TJ, Harrison RR, Lester HA, Masmanidis S (2011) Multiplexed, high density electrophysiology with nanofabricated neural probes. PLoS One 6(10), e26204
Favorov OV, Diamond ME (1990) Demonstration of discrete place-defined columns-segregates-in the cat SI. J Comp Neurol 298:97–112
Favorov OV, Diamond ME, Whitsel BL (1987) Evidence for a mosaic representation of the body surface in area 3b of the somatic cortex of cat. Proc Natl Acad Sci U S A 84(18):6606–6610
Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61(2):331–349
Fuster JM (2001) The prefrontal cortex–an update: time is of the essence. Neuron 30:319–333
Fuster JM (2007) Jackson and the frontal executive hierarchy. Int J Psychophysiol 64:106–107
Fuster JM, Bressler SL (2012) Cognit activation: a mechanism enabling temporal integration in working memory. Trends Cogn Sci 16(4):207–218
Gilbert CD, Wiesel TN (1989) Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci 9:2432–2442
Goldman-Rakic PS (1996) The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Philos Trans R Soc Lond B Biol Sci 351:1445–1453
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25
Hampson RE, Coates TD Jr, Gerhardt G,A, Deadwyler SA (2004) Ceramic-based micro-electrode neuronal recordings in the rat and monkey. Proc Annu Int Conf IEEE Eng Med Biol Soc (EMBS) 25:3700–3703
Hampson RE, Gerhardt GA, Marmarelis V, Song D, Opris I, Santos L, Berger TW, Deadwyler SA (2012) Facilitation and restoration of cognitive function in primate prefrontal cortex by a neuroprosthesis that utilizes minicolumn-specific neural firing. J Neural Eng 9(5):056012
Hansen BJ, Chelaru MI, Dragoi V (2012) Correlated variability in laminar cortical circuits. Neuron 76(3):590–602. doi:10.1016/j.neuron.2012.08.029
Hirabayashi T, Takeuchi D, Tamura K, Miyashita Y (2013a) Microcircuits for hierarchical elaboration of object coding across primate temporal areas. Science 341(6142):191–195
Hirabayashi T, Takeuchi D, Tamura K, Miyashita Y (2013b) Functional microcircuit recruited during retrieval of object association memory in monkey perirhinal cortex. Neuron 77(1):192–203
Hirata Y, Sawaguchi T (2008) Functional columns in the primate prefrontal cortex revealed by optical imaging in vitro. Neurosci Res 61(1):1–10
Hoover JE, Strick PL (1993) Multiple output channels in the basal ganglia. Science 259(5096):819–821
Horton JC, Adams DL (2005) The cortical column: a structure without a function. Philos Trans R Soc Lond B Biol Sci 360(1456):837–862
Hubel DH (1982) Cortical neurobiology: a slanted historical perspective. Annu Rev Neurosci 5:363–370
Hubel DH, Wiesel TN (1969) Anatomical demonstration of columns in the monkey striate cortex. Nature 221:747–750
Hubel DH, Wiesel TN (1974) Sequence regularity and geometry of orientation columns in the monkey striate cortex. J Comp Neurol 158(3):267–293
Jones EG (2000) Microcolumns in the cerebral cortex. A historical overview of the concept of micro- or minicolumns. Proc Natl Acad Sci U S A 97(10):5019–5021
Jones EG, Rakic P (2010) Radial columns in cortical architecture: it is the composition that counts. Cereb Cortex 20(10):2261–2264
Kaas JH (2012) Evolution of columns, modules, and domains in the neocortex of primates. Proc Natl Acad Sci U S A 109(Suppl 1):10655–10660
Katz LC, Gilbert CD, Wiesel TN (1989) Local circuits and ocular dominance columns in monkey striate cortex. J Neurosci 9:1389–1399
Kritzer MF, Goldman-Rakic PS (1995) Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey. J Comp Neurol 359:131–143
Leise EM (1990) Modular construction of nervous systems: a basic principle of design for invertebrates and vertebrates. Brain Res Brain Res Rev 15(1):1–23
Mahan MY, Georgopoulos AP (2013) Motor directional tuning across brain areas: directional resonance and the role of inhibition for directional accuracy. Front Neural Circ 7:92. doi:10.3389/fncir.2013.00092
McCulloch WS (1959) Agatha Tyche of nervous nets – the lucky reckoners. In: McCulloch WS (ed) Embodiments of mind. MIT Press, Cambridge, 1965, pp 203–215 (Reprint of: National Physical Laboratory. Mechanisation of thought processes. London: H.M. Stationery Office, pp 611–625)
McFarland NR, Haber SN (2002) Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. J Neurosci 22(18):8117–8132
Middleton FA, Strick PLB-g (2002) Projections to the prefrontal cortex of the primate. Cereb Cortex 12(9):926–935
Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202
Mo J, Schroeder CE, Ding M (2011) Attentional modulation of alpha oscillations in macaque inferotemporal cortex. J Neurosci 31(3):878–882
Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20:408–434
Mountcastle VB (1978) An organizing principle for cerebral function: the unit module and the distributed system. In: Edelman GM, Mountcastle VB (eds) The mindful brain. MIT Press, Cambridge, MA, pp 7–50
Mountcastle VB (1997) The columnar organization of the neocortex. A comprehensive review of the literature indicating the modular architecture of the cortex. Brain 120(4):701–722
Mountcastle VB (1998) Perceptual neuroscience. The cerebral cortex. Harvard University Press, Cambridge
Mountcastle VB (2003) Introduction. Cereb Cortex 13:2–4
Mountcastle VB, Berman A, Davies P (1955) Topographic organization and modality representation in the first somatic area of cat’s cerebral cortex by method of single unit analysis. Am J Physiol 183:464
Mountcastle VB, Berman AL, Davies P (1957) Response properties of neurons of cats’ somatic sensory cortex to peripheral stimuli. J Neurophysiol 20(4):374–407
Moxon KA, Leiser SC, Gerhardt GA, Barbee KA, Chapin JK (2004) Ceramic-based multisite electrode arrays for chronic single-neuron recording. IEEE Trans Biomed Eng 51:647–656
Naya Y, Suzuki WA (2011) Integrating what and when across the primate medial temporal lobe. Science 333:773–776
Opris I, Bruce CJ (2005) Neural circuitry of judgment and decision mechanisms. Brain Res Rev 48:509–526
Opris I, Barborica A, Ferrera VP (2001) A gap effect during microstimulation in the prefrontal cortex of monkeys. Exp Brain Res 138:1–7
Opris I, Barborica A, Ferrera VP (2005) Microstimulation of dorsolateral prefrontal cortex biases saccade target selection. J Cogn Neurosci 17(6):893–904
Opris I, Hampson RE, Deadwyler SA (2009) The encoding of cocaine vs. natural rewards in the striatum of nonhuman primates: categories with different activations. Neuroscience 163(1):40–54
Opris I, Hampson RE, Stanford TR, Gerhardt GA, Deadwyler SA (2011) Neural activity in frontal cortical cell layers: evidence for columnar sensorimotor processing. J Cogn Neurosci 23(6):1507–1521
Opris I, Santos LM, Song D, Gerhardt GA, Berger TW, Hampson RE, Deadwyler SA (2012a) Prefrontal cortical microcircuits bind perception to executive control. Sci Rep 2013 3:2285
Opris I, Hampson RE, Gerhardt GA, Berger TW, Deadwyler SA (2012b) Columnar processing in primate pFC: evidence for executive control microcircuits. J Cogn Neurosci 24(12):2334–2347
Opris I, Fuqua JL, Huettl PF, Gerhardt GA, Berger TW, Hampson RE, Deadwyler SA (2012c) Closing the loop in primate prefrontal cortex: inter-laminar processing. Front Neural Circuits 6:88
Opris I et al (2012d) Closing the loop in primate prefrontal cortex: inter-laminar processing. Front Neurosci 6
Opris I, Santos L, Gerhardt GA et al (2013) Prefrontal cortical microcircuits bind perception to executive control. Sci Rep 3:2285. doi:10.1038/srep02285
Posner M, Snyder C (1975) Attention and cognitive control. In: Solso R (ed) Information processing and cognition: the Loyola symposium. Lawrence Erlbaum, Hillsdale
Quintana J, Fuster JM (1999) From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cereb Cortex 9:213–221
Raghanti MA, Spocter MA, Butti C, Hof PR, Sherwood CC (2010) A comparative perspective on minicolumns and inhibitory GABAergic interneurons in the neocortex. Front Neuroanat 4:3
Rakic P (1988) Specification of cerebral cortical areas. Science 241(4862):170–176
Rakic P (2008) Confusing cortical columns. Proc Natl Acad Sci U S A 105(34):12099–12100
Rao SC, Rainer G, Miller EK (1997) Integration of what and where in the primate prefrontal cortex. Science 276:821–824
Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81:1903–1916
Ratcliff R, Cherian A, Segraves M (2003) A comparison of macaque behavior and superior colliculus neuronal activity to predictions from models of two-choice decisions. J Neurophysiol 90(3):1392–1407
Rinkus GJ (2010) A cortical sparse distributed coding model linking mini- and macrocolumn-scale functionality. Front Neuroanat 4:17
Romo R, Hernández A, Zainos A, Lemus L, Brody CD (2002) Neuronal correlates of decision-making in secondary somatosensory cortex. Nat Neurosci 5(11):1217–1225
Salinas E (2004) Fast remapping of sensory stimuli onto motor actions on the basis of contextual modulation. J Neurosci 24(5):1113–1118
Selemon LD, Goldman-Rakic PS (1988) Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J Neurosci 8:4049–4068
Shallice T, Burgess PW (1991) Deficits in strategy application following frontal lobe damage in man. Brain 114(2):727–741
Shallice T, Burgess P (1996) The domain of supervisory processes and temporal organization of behaviour. Philos Trans R Soc Lond B Biol Sci 351:1405–1411
Shepherd G, Grillner S (2010) Handbook of brain microcircuits. Oxford University Press, New York
Sokhadze E et al (2010) Impaired error monitoring and correction function in autism. J Neurother 14:79–95
Sokhadze E et al (2012) Prefrontal neuromodulation using rTMS improves error monitoring and correction function in autism. Appl Psychophysiol Biofeedback 37:91–102
Suyatin DB, Hallstram W, Samuelson L, Montelius L, Prinz CN, Kanje M (2009) Gallium phosphide nanowire arrays and their possible application in cellular force investigations. J Vac Sci Technol B 27:3092–3094
Swadlow HA, Gusev AG, Bezdudnaya T (2002) Activation of a cortical column by a thalamocortical impulse. J Neurosci 22:7766–7773
Swindale NV (1998) Cortical organization: modules, polymaps and mosaics. Curr Biol 8:R270–R273
Swindale NV, Shoham D, Grinvald A, Bonhoeffer T, Hübener M (2000) Visual cortex maps are optimized for uniform coverage. Nat Neurosci 3:822–826
Szentágothai J, Arbib MA (1975) Conceptual models of neural organization. MIT Press, Cambridge, MA
Takeuchi D, Hirabayashi T, Tamura K, Miyashita Y (2011) Reversal of interlaminar signal between sensory and memory processing in monkey temporal cortex. Science 331:1443–1447
Thomson AM, Bannister AP (2003) Interlaminar connections in the neocortex. Cereb Cortex 13(1):5–14
Tomasi D, Volkow ND et al (2010) Disrupted functional connectivity with dopaminergic midbrain in cocaine abusers. PLoS One 5:e10815
Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT, Cambridge, MA, pp 549–586
Van Essen DC, Newsome WT, Bixby JL (1982) The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey. J Neurosci 2(3):265–283
Viventi J, Kim D-H, Vigeland L, Frechette ES, Blanco JA, Kim Y-S, Avrin AE, Tiruvadi VR, Hwang S-W, Vanleer AC, Wulsin DF, Davis K, Gelber CE, Palmer L, Van der Spiegel J, Wu J, Xiao J, Huang Y, Contreras D, Rogers JA, Litt B (2011) Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo. Nat Neurosci 14:1599–1605
Wang XJ (2012) Neural dynamics and circuit mechanisms of decision-making. Curr Opin Neurobiol 22(6):1039–1046
Wang M et al (2011) Neuronal basis of age-related working memory decline. Nature 476:210–213
Weiler N, Wood L, Yu J, Solla SA, Shepherd GM (2008) Top-down laminar organization of the excitatory network in motor cortex. Nat Neurosci 11:360–366
Wiesel TN, Hubel DH (1974) Ordered arrangement of orientation columns in monkeys lacking visual experience. J Comp Neurol 158(3):307–318
Wilson FA, O’Scalaidhe SP, Goldman-Rakic PS (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260:1955–1958
Zhang M, Alloway KD (2006) Intercolumnar synchronization of neuronal activity in rat barrel cortex during patterned airjet stimulation: a laminar analysis. Exp Brain Res 169(3):311–325
Zorzos AN, Scholvin J, Boyden ES, Fonstad CG (2012) Three-dimensional multiwaveguide probe array for light delivery to distributed brain circuits. Opt Lett 37:4841–4843
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Opris, I., Popa, I.L., Casanova, M.F. (2015). Prefrontal Cortical Microcircuits for Executive Control of Behavior. 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_10
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