Rule Activity Related to Spatial and Numerical Magnitudes: Comparison of Prefrontal, Premotor, and Cingulate Motor Cortices

Abstract

In everyday situations, quantitative rules, such as "greater than/less than," need to be applied to a multitude of magnitude comparisons, be they sensory, spatial, temporal, or numerical. We have previously shown that rules applied to different magnitudes are encoded in the lateral PFC. To investigate if and how other frontal lobe areas also contribute to the encoding of quantitative rules applied to multiple magnitudes, we trained monkeys to switch between "greater than/less than" rules applied to either line lengths (spatial magnitudes) or dot numerosities (discrete numerical magnitudes). We recorded single-cell activity from the dorsal premotor cortex (dPMC) and cingulate motor cortex (CMA) and compared it with PFC activity. We found the largest proportion of quantitative rule-selective cells in PFC (24% of randomly selected cells), whereas neurons in dPMC and CMA rarely encoded the rule (6% of the cells). In addition, rule selectivity of individual cells was highest in PFC neurons compared with dPMC and CMA neurons. Rule-selective neurons that simultaneously represented the "greater than/less than" rules applied to line lengths and numerosities ("rule generalists") were exclusively present in PFC. In dPMC and CMA, however, neurons primarily encoded rules applied to only one of the two magnitude types ("rule specialists"). Our data suggest a special involvement of PFC in representing quantitative rules at an abstract level, both in terms of the proportion of neurons engaged and the coding capacities.

Single-cell coding of sensory, spatial and numerical magnitudes in primate prefrontal, premotor and cingulate motor cortices

“…In the current study, we find that neurons in PMd and CMA are not (more than expected by chance) encoding magnitudes during the sample and delay periods. In addition, only a very small portion (6 %) of cells in CMA and PMd encoded the rule (Eiselt and Nieder 2014). This is in contrast to 24 % of rule-selective cells (Eiselt and Nieder 2014) and 25 % of sample-selective cells (current study) in the PFC.…”

“…In addition, only a very small portion (6 %) of cells in CMA and PMd encoded the rule (Eiselt and Nieder 2014). This is in contrast to 24 % of rule-selective cells (Eiselt and Nieder 2014) and 25 % of sample-selective cells (current study) in the PFC. In the current study, we found that 25 % of all recorded neurons in PFC exhibited sample selectivity for either spatial frequency, line length or numerosity stimuli, with a similar number of neurons representing each of the three different magnitude types.…”

“…Alternatively, the lateral prefrontal cortex (PFC), which is known for its involvement in quantity processing (e.g., Genovesio et al 2005Genovesio et al , 2009Genovesio et al , 2011Hayashi et al 2013;Nieder 2013;Nieder and Miller 2004;Onoe et al 2001;Piazza et al 2007;Rao et al 2001;Tudusciuc and Nieder 2009), might be a special key area in integrating quantitative information. The combined results from the current and a previous study (Eiselt and Nieder 2014) suggest a privileged position of the PFC in encoding magnitude and rule information in a rule-guided magnitude discrimination task. In the current study, we find that neurons in PMd and CMA are not (more than expected by chance) encoding magnitudes during the sample and delay periods.…”

“…Neurons in CMA of monkey O were recorded either anterior (CMAr) or posterior (CMAd) to the genu of the arcuate sulcus (dashed line in Fig. 3d, right panel), whereas only CMAr neurons were recorded from monkey E (see also Eiselt and Nieder 2014). Since no sample-selective neurons were found in CMAr and CMAd of monkey O, CMA is equivalent to CMAr in the current study.…”

“…No signals were detected at depths ranging from 5 to 7 mm below the cortical surface, indicating that our recording sites were lateral to the medial wall. The positions of the recording chambers were calculated using stereotaxic coordinates and were reconstructed using MRI images of both monkeys (Eiselt and Nieder 2014). Arrays of eight glass-coated tungsten microelectrodes of 1-MΩ impedance (Alpha Omega) were used and lowered into the brain through a grid with 1 mm spacing using custom-made microdrives.…”