Neural Activity in Frontal Cortical Cell Layers: Evidence for Columnar Sensorimotor Processing

Abstract

The mammalian frontal cortex (FCx) is at the top of the brain’s sensorimotor hierarchy and includes cells in the supragranular Layer 2/3, which integrate convergent sensory information for transmission to infragranular Layer 5 cells to formulate motor system outputs that control behavioral responses. Functional interaction between these two layers of FCx was examined using custom-designed ceramic-based microelectrode arrays (MEAs) that allowed simultaneous recording of firing patterns of FCx neurons in Layer 2/3 and Layer 5 in nonhuman primates performing a simple go/no-go discrimination task. This unique recording arrangement showed differential encoding of task-related sensory events by cells in each layer with Layer 2/3 cells exhibiting larger firing peaks during presentation of go target and no-go target task images, whereas Layer 5 cells showed more activity during reward contingent motor responses in the task. Firing specificity to task-related events was further demonstrated by synchronized firing between pairs of cells in different layers that occupied the same vertically oriented “column” on the MEA. Pairs of cells in different layers recorded at adjacent “noncolumnar” orientations on the MEA did not show synchronized firing during the same task-related events. The results provide required evidence in support of previously suggested task-related sensorimotor processing in the FCx via functionally segregated minicolumns.

Periodic Organization of a Major Subtype of Pyramidal Neurons in Neocortical Layer V

“…Such organization is found in multiple cortical areas including the visual Wiesel, 1974, 1977;Ohki et al, 2006;Kara and Boyd, 2009), somatosensory (Bruno et al, 2003;Andermann and Moore, 2006), motor (Amirikian and Georgopoulos, 2003;Georgopoulos et al, 2007;Dombeck et al, 2009;Komiyama et al, 2010), and frontal cortex (Opris et al, 2011). Our results suggest that cortical functions performed within tens of micrometers in the tangential orientation may be processed by local circuits with a periodic neuronal distribution.…”

Dopamine’s Actions in Primate Prefrontal Cortex: Challenges for Treating Cognitive Disorders

“…The Response cells likely reside in layer V, because this layer is the focus of neurons that synthesize D2R (Lidow et al, 1989), and Response-related firing has been recorded from deeper rather than superficial layers in similar cognitive tasks (Opris et al, 2011). The postsaccadic "feedback" Response cells are activated by AMPAR stimulation in addition to NMDAR , and systemic ketamine increases their firing, similar to what is described in rodents (Jackson et al, 2004).…”

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).…”

“…MEAs with 4-16 recording sites have been fabricated with recording sites ranging from 10 Â 10 μm to 15 Â 330 μm. Various recording site sizes and arrangements have been selected to conform to specific brain layers, which we now term biomorphic (Burmeister et al 2002;Moxon et al 2004;Opris et al 2011;Stephens et al 2010). The front and back of the ceramic substrate can be patterned to increase recording site density and create isolated front and back site pairs.…”

“…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.…”