Columnar Processing in Primate pFC: Evidence for Executive Control Microcircuits

Abstract

A common denominator for many cognitive disorders of human brain is the disruption of neural activity within pFC, whose structural basis is primarily interlaminar (columnar) microcircuits or “mini-columns.” The importance of this brain region for executive decision-making has been well documented; however, because of technological constraints, the minicolumnar basis is not well understood. Here, via implementation of a unique conformal multielectrode recording array, the role of interlaminar pFC minicolumns in the executive control of task-related target selection is demonstrated in nonhuman primates performing a visuomotor DMS task. The results reveal target-specific, interlaminar correlated firing during the decision phase of the trial between multielectrode recording array-isolated minicolumnar pairs of neurons located in parallel in layers 2/3 and layer 5 of pFC. The functional significance of individual pFC minicolumns (separated by 40 μm) was shown by reduced correlated firing between cell pairs within single minicolumns on error trials with inappropriate target selection. To further demonstrate dependence on performance, a task-disrupting drug (cocaine) was administered in the middle of the session, which also reduced interlaminar firing in minicolumns that fired appropriately in the early (nondrug) portion of the session. The results provide a direct demonstration of task-specific, real-time columnar processing in pFC indicating the role of this type of microcircuit in executive control of decision-making in primate brain.

Right frontal stroke: extra-frontal lesions, executive functioning and impulsive behaviour

“…Processes essential to EF such as monitoring and selecting information depend on brain circuits which integrate and select information such as the temporal lobe, parietal lobe, striatum and sub-cortical structures (Fuster and Bressler 2012). Evidence indicates that the basal ganglia are part of connected with the frontal cortical regions (Middleton and Strick 2002) and play a role in executive decisions (Opris et al 2012a(Opris et al , 2012b.…”

The Function of Cortical Microcircuits: Insights from Biomorphic Ceramic-Based Microelectrode Arrays

“…Previous anatomic and electrophysiological investigations (Buxhoeveden and Casanova 2002;Casanova et al 2002aCasanova et al , b, 2003Casanova et al , 2011Opris et al 2011;González-Burgos et al 2000;Kritzer and Goldman-Rakic 1995) have examined both the structural and the functional bases of this operation (de Kock et al 2007;Sakurai and Takahashi 2006;Opris et al 2005), but only a few studies have examined simultaneous firing patterns of cells in different cortical layers (Derdikman et al 2006;Zhang and Alloway 2006;Krupa et al 2004;Jung et al 1998;Opris et al 2012aOpris et al , 2013Takeuchi et al 2011). However, in the last few years, a new approach for studying columnar/laminar structure and functionality of the brain has emerged (Opris et al 2011(Opris et al , 2012a(Opris et al , b, 2013Constantinople and Bruno 2013;Hansen et al 2012;Takeuchi et al 2011;Mahan and Georgopoulos 2013).…”

“…These arrays were capable of recording single neuron activity from each of their recording sites for at least 6 months during chronic implantation in the somatosensory cortex of rats (Moxon et al 2004), and monkey hippocampus (Hampson et al 2013a) as well as in the prefrontal cortex of nonhuman primates (Opris et al 2011(Opris et al , 2012a. The vertical arrangement of the recording sites on these biomorphic MEAs is ideal for simultaneously recording across the different layers of brain areas such as the cerebral cortex and hippocampus in chronic preparations (Opris et al 2011(Opris et al , 2012a(Opris et al , b, 2013Hampson et al 2012bHampson et al , 2013a.…”

“…The vertical arrangement of the recording sites on these biomorphic MEAs is ideal for simultaneously recording across the different layers of brain areas such as the cerebral cortex and hippocampus in chronic preparations (Opris et al 2011(Opris et al , 2012a(Opris et al , b, 2013Hampson et al 2012bHampson et al , 2013a. Hippocampal pyramidal cells in the rat have been stimulated and recorded (Hampson et al 2013a).…”

“…Although the acceptable ratio of signal-to-noise is 2:1 for most recordings, the ratios for single and multiple neuron firing recordings with MEAs typically range between 3:1 and 10:1, in both rodent and nonhuman primates (Opris et al 2011(Opris et al , 2012a. For in vivo electrochemical recording, MEA recordings achieve improved signal-to-noise by self-referencing noise subtraction (Burmeister and Gerhardt 2001), but can detect changes in glutamate as low as 0.1 μM/s.…”