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Functional constraints in the evolution of brain circuits.

Bosman CA, Aboitiz F - Front Neurosci (2015)

Bottom Line: Accordingly, these oscillatory interactions are observed across multiple brain scale levels, and they are associated with several sensory, motor, and cognitive processes.Most notably, oscillatory interactions are also found in the complete spectrum of vertebrates.We argue that isocortex architectures represent canonical microcircuits resulting from: (i) the early selection of neuronal architectures based on the oscillatory excitatory-inhibitory balance, which lead to the implementation of compartmentalized oscillations and (ii) the subsequent emergence of inferential coding strategies (predictive coding), which are able to expand computational capacities.

View Article: PubMed Central - PubMed

Affiliation: Cognitive and Systems Neuroscience Group, Swammerdam Institute for Life Sciences, Center for Neuroscience, Faculty of Science, University of Amsterdam Amsterdam, Netherlands ; Facultad de Ciencias de la Salud, Universidad Autónoma de Chile Santiago, Chile.

ABSTRACT
Regardless of major anatomical and neurodevelopmental differences, the vertebrate isocortex shows a remarkably well-conserved organization. In the isocortex, reciprocal connections between excitatory and inhibitory neurons are distributed across multiple layers, encompassing modular, dynamical and recurrent functional networks during information processing. These dynamical brain networks are often organized in neuronal assemblies interacting through rhythmic phase relationships. Accordingly, these oscillatory interactions are observed across multiple brain scale levels, and they are associated with several sensory, motor, and cognitive processes. Most notably, oscillatory interactions are also found in the complete spectrum of vertebrates. Yet, it is unknown why this functional organization is so well conserved in evolution. In this perspective, we propose some ideas about how functional requirements of the isocortex can account for the evolutionary stability observed in microcircuits across vertebrates. We argue that isocortex architectures represent canonical microcircuits resulting from: (i) the early selection of neuronal architectures based on the oscillatory excitatory-inhibitory balance, which lead to the implementation of compartmentalized oscillations and (ii) the subsequent emergence of inferential coding strategies (predictive coding), which are able to expand computational capacities. We also argue that these functional constraints may be the result of several advantages that oscillatory activity contributes to brain network processes, such as information transmission and code reliability. In this manner, similarities in mesoscale brain circuitry and input-output organization between different vertebrate groups may reflect evolutionary constraints imposed by these functional requirements, which may or may not be traceable to a common ancestor.

No MeSH data available.


Related in: MedlinePlus

(A) Laminar recording on visual cortex using a linear microelectrode array (LMA). (B) Stimulus-evoked current source density (CSD) analysis using laminar probes. LMAs typically depict sinks (cation inflow from the extracellular to the intracellular space, in red) and sources (cation outflow from the intracellular to the extracellular space, in blue) of neuronal activity. This configuration pattern is useful to segregate differential layer activity. (C) Noise correlation amplitude is significantly lower in granular layers as compared with supra and infragranular layers. Black and gray bars denote two different monkeys. (B,C) adapted from Hansen et al. (2012). (D) Decrease of noise correlations amplitude in cyto-architectonically defined intermediate layers of the songbird auditory caudal meso/nidopallium cortex [Asteriks indicate significant differences in correlations between regions (p < 0.05, Kruskal-Wallis test with multiple comparisons correction)]. Adapted from Calabrese and Woolley (2015).
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Figure 2: (A) Laminar recording on visual cortex using a linear microelectrode array (LMA). (B) Stimulus-evoked current source density (CSD) analysis using laminar probes. LMAs typically depict sinks (cation inflow from the extracellular to the intracellular space, in red) and sources (cation outflow from the intracellular to the extracellular space, in blue) of neuronal activity. This configuration pattern is useful to segregate differential layer activity. (C) Noise correlation amplitude is significantly lower in granular layers as compared with supra and infragranular layers. Black and gray bars denote two different monkeys. (B,C) adapted from Hansen et al. (2012). (D) Decrease of noise correlations amplitude in cyto-architectonically defined intermediate layers of the songbird auditory caudal meso/nidopallium cortex [Asteriks indicate significant differences in correlations between regions (p < 0.05, Kruskal-Wallis test with multiple comparisons correction)]. Adapted from Calabrese and Woolley (2015).

Mentions: The understanding of the neuronal dynamics generated in canonical microcircuits has been facilitated by the popularization of techniques that enable simultaneous recordings through multiple areas and cortical layers (Lewis et al., 2015). Linear microelectrode (LMAs) feature several contact points through one or multiple shanks (Figure 2A). This configuration facilitates recordings of neuronal activity—spikes and local field potentials (LFP)—simultaneously across layers. In animals, high-density electrocorticograms (ECoGs) arrays can be used to study cortical LFP-LFP interactions across different brain areas. In LMAs, LFPs are usually studied using current source density (CSD) analysis, a technique amendable to give access to the sinks and sources of voltage differences at the extracellular space (Mitzdorf, 1985). CSD analysis can be used to identify electrode position based on the different profiles obtained at different layers (Figure 2B). Additionally, the temporal coordination between spikes and LFPs can be described using spike-field coherence based techniques, which quantify the phase relationships between the ongoing LFP and spike activity. All these techniques are especially advantageous for the study of long-range interactions across cortical microcircuits (Lewis et al., 2015).


Functional constraints in the evolution of brain circuits.

Bosman CA, Aboitiz F - Front Neurosci (2015)

(A) Laminar recording on visual cortex using a linear microelectrode array (LMA). (B) Stimulus-evoked current source density (CSD) analysis using laminar probes. LMAs typically depict sinks (cation inflow from the extracellular to the intracellular space, in red) and sources (cation outflow from the intracellular to the extracellular space, in blue) of neuronal activity. This configuration pattern is useful to segregate differential layer activity. (C) Noise correlation amplitude is significantly lower in granular layers as compared with supra and infragranular layers. Black and gray bars denote two different monkeys. (B,C) adapted from Hansen et al. (2012). (D) Decrease of noise correlations amplitude in cyto-architectonically defined intermediate layers of the songbird auditory caudal meso/nidopallium cortex [Asteriks indicate significant differences in correlations between regions (p < 0.05, Kruskal-Wallis test with multiple comparisons correction)]. Adapted from Calabrese and Woolley (2015).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4555059&req=5

Figure 2: (A) Laminar recording on visual cortex using a linear microelectrode array (LMA). (B) Stimulus-evoked current source density (CSD) analysis using laminar probes. LMAs typically depict sinks (cation inflow from the extracellular to the intracellular space, in red) and sources (cation outflow from the intracellular to the extracellular space, in blue) of neuronal activity. This configuration pattern is useful to segregate differential layer activity. (C) Noise correlation amplitude is significantly lower in granular layers as compared with supra and infragranular layers. Black and gray bars denote two different monkeys. (B,C) adapted from Hansen et al. (2012). (D) Decrease of noise correlations amplitude in cyto-architectonically defined intermediate layers of the songbird auditory caudal meso/nidopallium cortex [Asteriks indicate significant differences in correlations between regions (p < 0.05, Kruskal-Wallis test with multiple comparisons correction)]. Adapted from Calabrese and Woolley (2015).
Mentions: The understanding of the neuronal dynamics generated in canonical microcircuits has been facilitated by the popularization of techniques that enable simultaneous recordings through multiple areas and cortical layers (Lewis et al., 2015). Linear microelectrode (LMAs) feature several contact points through one or multiple shanks (Figure 2A). This configuration facilitates recordings of neuronal activity—spikes and local field potentials (LFP)—simultaneously across layers. In animals, high-density electrocorticograms (ECoGs) arrays can be used to study cortical LFP-LFP interactions across different brain areas. In LMAs, LFPs are usually studied using current source density (CSD) analysis, a technique amendable to give access to the sinks and sources of voltage differences at the extracellular space (Mitzdorf, 1985). CSD analysis can be used to identify electrode position based on the different profiles obtained at different layers (Figure 2B). Additionally, the temporal coordination between spikes and LFPs can be described using spike-field coherence based techniques, which quantify the phase relationships between the ongoing LFP and spike activity. All these techniques are especially advantageous for the study of long-range interactions across cortical microcircuits (Lewis et al., 2015).

Bottom Line: Accordingly, these oscillatory interactions are observed across multiple brain scale levels, and they are associated with several sensory, motor, and cognitive processes.Most notably, oscillatory interactions are also found in the complete spectrum of vertebrates.We argue that isocortex architectures represent canonical microcircuits resulting from: (i) the early selection of neuronal architectures based on the oscillatory excitatory-inhibitory balance, which lead to the implementation of compartmentalized oscillations and (ii) the subsequent emergence of inferential coding strategies (predictive coding), which are able to expand computational capacities.

View Article: PubMed Central - PubMed

Affiliation: Cognitive and Systems Neuroscience Group, Swammerdam Institute for Life Sciences, Center for Neuroscience, Faculty of Science, University of Amsterdam Amsterdam, Netherlands ; Facultad de Ciencias de la Salud, Universidad Autónoma de Chile Santiago, Chile.

ABSTRACT
Regardless of major anatomical and neurodevelopmental differences, the vertebrate isocortex shows a remarkably well-conserved organization. In the isocortex, reciprocal connections between excitatory and inhibitory neurons are distributed across multiple layers, encompassing modular, dynamical and recurrent functional networks during information processing. These dynamical brain networks are often organized in neuronal assemblies interacting through rhythmic phase relationships. Accordingly, these oscillatory interactions are observed across multiple brain scale levels, and they are associated with several sensory, motor, and cognitive processes. Most notably, oscillatory interactions are also found in the complete spectrum of vertebrates. Yet, it is unknown why this functional organization is so well conserved in evolution. In this perspective, we propose some ideas about how functional requirements of the isocortex can account for the evolutionary stability observed in microcircuits across vertebrates. We argue that isocortex architectures represent canonical microcircuits resulting from: (i) the early selection of neuronal architectures based on the oscillatory excitatory-inhibitory balance, which lead to the implementation of compartmentalized oscillations and (ii) the subsequent emergence of inferential coding strategies (predictive coding), which are able to expand computational capacities. We also argue that these functional constraints may be the result of several advantages that oscillatory activity contributes to brain network processes, such as information transmission and code reliability. In this manner, similarities in mesoscale brain circuitry and input-output organization between different vertebrate groups may reflect evolutionary constraints imposed by these functional requirements, which may or may not be traceable to a common ancestor.

No MeSH data available.


Related in: MedlinePlus