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Inter-Laminar Microcircuits Across Neocortex: Repair and Augmentation

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Inter-Laminar Microcircuits Across Neocortex: Repair and Augmentation View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Frontiers - Publisher Connector OPINION ARTICLE published: 19 November 2013 SYSTEMS NEUROSCIENCE doi: 10.3389/fnsys.2013.00080 Inter-laminar microcircuits across neocortex: repair and augmentation Ioan Opris* Department of Physiology and Pharmacology, Wake Forest University School of Medicine, Winston-Salem, NC, USA *Correspondence: [email protected] Edited by: Mikhail Lebedev, Duke University, USA Reviewed by: Manuel Casanova, University of Louisville, USA Keywords: cortical minicolumn, cortical layer, cortical module, microcircuit, neocortex, repair, brain machine interface, prosthetics INTRODUCTION thalamus (Constantinople and Bruno, of microcolumns are specific to particular Repair and brain augmentation 2013). The supra-granular layers consist cortical areas. For example, the thickness approaches, such as brain-machine inter- of small pyramidal neurons that form a of L4 is different across areas (DeFelipe faces, neural stimulation and other neural complex network of intra-cortical connec- et al., 2012). It is most prominent in sen- prostheses, have experienced a rapid devel- tions, particularly the connections to the sory areas and the thinnest in the motor opment during the last decade (Nicolelis infra-granular layers of larger pyramidal cortex. There are also area-specific differ- et al., 2003; Lebedev and Nicolelis, 2006). neurons that generate most of the output ences in the topographic connectivity of Still, only few of these methods target the from cerebral cortex to other parts of the microcircuits with their cortical and sub- fine microcircuitry of the brain (Jones and brain (Buxhoeveden and Casanova, 2002). cortical projection areas (Das and Gilbert, Rakic, 2010; Opris et al., 2012a). Here, it According to this three stratum functional 1995; Kritzer and Goldman-Rakic, 1995; is highlighted the potential employing of module, infra-granular layers execute the Opris et al., 2013). inter-laminar recording and microstim- associative computations elaborated in ulation of cortical microcircuits to build supra-granular layers (Buxhoeveden and INTER-AREA CONNECTIVITY neural prostheses for repair and augmen- Casanova, 2002; Casanova et al., 2011). Cortical microcircuits are connected into tationofcognitivefunction.Inthefuture, Here, the focus is on inter-laminar a macro-network by cortico-cortical con- such microcircuit-based prostheses will cortical microcircuits formed by inter- nections, which link areas within the same provide efficient therapies for patients connected pyramidal neurons from the hemisphere, as well as between hemi- with neurological and psychiatric disor- supra-granular and infra-granular layers spheres (Van Essen et al., 1982). This ders. Moreover, it is implied that neural (Thomson and Bannister, 2003; Opris super network subserves the “perception- enhancement approaches can be applied et al., 2011, 2012a,b, 2013). These micro- to-action” cycle—a group of processes that to inter-laminar microcircuits across the circuits receive input from neurons in layer handle environmental stimuli and con- entire cortex. L4, which project to L2/3, or through vert them into actions (Romo et al., 2002; direct thalamic projections to the supra- Fuster and Bressler, 2012). Microcircuits CORTICAL MICROCIRCUITS granular layers in the higher-order cortical within the same hemisphere are intercon- As proposed by Mountcastle, the pri- areas. Neurons in L2/3 then project top- nected (from low level sensory to high mate neocortical circuitry has a modular down to L5, where they target specific level associative processes) through hori- architecture that subserves a multitude of types of pyramidal cells and inhibitory zontal connections in lamina 2/3, span- sensory (visual, auditory, touch), motor, interneurons. Some L5 neurons project ning over many cortical areas (Das and cognitive (attention, memory, decision) back to L2/3 neurons, forming an inter- Gilbert, 1995; Kritzer and Goldman-Rakic, and emotional functions (Mountcastle, laminar loop (Weiler et al., 2008)or 1995; Fuster and Bressler, 2012). 1957, 1997; Opris and Bruce, 2005; back to L4, targeting mostly interneurons Inter-area connectivity of cortical Shepherd and Grillner, 2010). These (Thomson and Bannister, 2003). The out- microcircuits preserves spatial topog- modules are composed of elemen- puts from cortical microcircuits, cortico- raphy suggesting a column-to-column tary building blocks formed by vertical striatal projections arise mostly from L5, match from one area to another (e.g., arrangements of cortical neurons, called whereas cortico-thalamic projections arise Figure 1B schematics of V1 projections minicolumns (Szentágothai and Arbib, from L6. to prefrontal area 46 through the dor- 1975; Mountcastle, 1997). Within mini- Cortical microcircuits are strikingly sal visual stream; Goldman-Rakic, 1996). columns, cortical neurons are aggregated similar across the neocortex (hence the Additionally, the topography is preserved into six horizontal layers (or laminae): term “canonical microcircuits”). It has within minicolumns owing to the inter- three supra-granular layers (L1-L3), a been suggested that such repeatability laminar projections (Opris et al., 2013). granular layer (L4) and two infra-granular in the microcircuit pattern plays a key Interhemispheric connectivity is formed layers (L5/L6) (Figure 1A). The gran- role in reducing the errors of encoding by neural interconnections of lamina 3b ular layer receives sensory input from (Bastos et al., 2012). Some characteristics (Jones et al., 1979; Van Essen et al., 1982). Frontiers in Systems Neuroscience www.frontiersin.org November 2013 | Volume 7 | Article 80 | 1 Opris Inter-laminar microcircuits across neocortex FIGURE 1 | Inter-Laminar Microcircuits across the Neocortex. (A) Cortical layers. Cross-correlation show that inter-laminar firing increased following minicolumn with pyramidal cells labeled in dark blue for supra-granular the presentation of targets compared to pre-target epoch. Recording array layers and red for infra-granular layers. Stellate cells in layer 4 are colored with the MIMO model for recording in layer 2/3 and stimulation in layer 5. in pink. The “curtain of inhibition” is depicted by interneurons, colored in Stimulation effect compare the population tuning for MIMO stim (red) vs. yellow. (B) Primate brain showing the cortical mantle split in cortical layers layer 5 prefrontal cortical activity (dark blue dotted line). Overall MIMO and minicolumns. Minicolumn across neocortex work cooperatively to stimulation effect (red) is significantly greater than no-stim and the chance translate perception into complex action. (C) Interlaminar recording of level (with permission from Opris et al., 2012a,b, 2013). (D) Nanoarray for pyramidal cells and MIMO stimulation model. Rasters and peri-event recording neural activity in cortical layers and minicolumns (with histograms in blue and red depict the activity of supra-and infra-granular permission from Alivisatos et al., 2013). ∗∗p < 0.001, ANOVA. MICROCIRCUITS AND COGNITION elementary computations related to exec- ofKentucky,examinedtheexecutivefunc- Recent research conducted in non-human utive control are performed by microcir- tion of prefrontal microcircuits (Opris primates indicates that a variety of sen- cuits in the prefrontal cortex (Opris et al., et al., 2012a,b, 2013). We trained rhe- sory, motor and executive functions 2012a,b), whereas microcircuits of the sus monkeys to select a target (spatial emerge from the interactions between temporal cortex maintain long term mem- or object) for hand movement, after a frontal, parietal, temporal and occipi- ory (Takeuchi et al., 2011; Hirabayashi memory delay, while the neural activity tal cortical microcircuits (Atencio and et al., 2013a). Prefrontal microcircuits are in prefrontal microcircuits was recorded Schreiner, 2010; Buffalo et al., 2011; in a unique and privileged position at (Figure 1C). Our electrode arrays were Takeuchi et al., 2011; Hansen et al., 2012; the top of sensory-to-motor hierarchy net- specifically designed to record from neu- Opris et al., 2012a,b, 2013; Hirabayashi work because they coordinate a multitude rons located in both supra- & infra- et al., 2013a,b; Mahan and Georgopoulos, of stimuli, perceptions, biases and actions granular layers of adjacent minicolumns. 2013). Moreover, several augmentation related to such functions as attention, deci- We analyzed correlated firing in neu- approaches based on microcircuits have sion making, and working memory. As rons from the supra- and infra-granular been implemented. These advances have such, prefrontal microcicuits integrate and layers. Interestingly, the extent of cor- been possible owing to the development synthetize signals over a broad spectrum of related firing was linked to the accu- of new multi-electrode arrays (MEA) fit- perceptual stimuli and various modalities. racy of monkey performance. Correlated ted for recordings from neural elements This integration is performed in supra- firing between cell pairs within single of cortical columns (Moxon et al., 2004). granular layers, whereas the output of the minicolumns was higher during correct Thus, MEAs with linear or bi-linear geom- infra-granular layers provides selection- selections and reduced in error trials etry have been successfully employed for related signals, which are sent back to the (Opris et al., 2012a). Thus, we discov- simultaneous recordings from supra- and
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