Comparison of abstract decision encoding in the monkey prefrontal cortex, the presupplementary, and cingulate motor areas

Abstract

Deciding between alternatives is a critical element of flexible behavior. Perceptual decisions have been studied extensively in an action-based framework. Recently, we have shown that abstract perceptual decisions are encoded in prefrontal cortex (PFC) neurons (Merten and Nieder 2012). However, the role of other frontal cortex areas remained elusive. Here, we trained monkeys to perform a rule-based visual detection task that disentangled abstract perceptual decisions from motor preparation. We recorded the single-neuron activity in the presupplementary (preSMA) and the rostral part of the cingulate motor area (CMAr) and compared it to the results previously found in the PFC. Neurons in both areas traditionally identified with motor planning process the abstract decision independently of any motor preparatory activity by similar mechanisms as the PFC. A larger proportion of decision neurons and a higher strength of decision encoding was found in the preSMA than in the PFC. Neurons in both areas reliably predicted the monkeys' decisions. The fraction of CMAr decision neurons and their strength of the decision encoding were comparable to the PFC. Our findings highlight the role of both preSMA and CMAr in abstract cognitive processing and emphasize that both frontal areas encode decisions prior to the preparation of a motor output.

Dopamine Regulates Two Classes of Primate Prefrontal Neurons That Represent Sensory Signals

“…The animals were trained to detect the stimuli and report their subjective perceptual judgment about the presence or absence of visual stimulation (Merten and Nieder, 2012) (Fig. 1a).…”

“…Here, we investigate in trained rhesus monkeys how DA controls the prefrontal representation of such brief sensory stimuli that must be detected by the animals (Merten andNieder, 2012, 2013). We found that DA strengthens visual signals by modulating activity in two distinct classes of neurons.…”

“…To determine whether DA modulated a signal metric, multiple linear regression analysis was applied to the population data (Merten and Nieder, 2012). Linear functions were fitted to the factors normalized visual contrast and iontophoresis condition (control and DA) using the model for the signal metric ( S): S ϭ a_0 ϩ a_stim ϫ STIM ϩ a_ion ϫ ION, where a_stim and a_ion are the coefficients that quantify the signal metric dependence on the normalized stimulus contrast (STIM) and the iontophoresis condition (ION).…”

“…The PFC collects this sensory information to form subjective judgments, such as regarding the presence or absence of sensory stimulation (de Lafuente and Romo, 2006). Recent electrophysiological studies have demonstrated that the physical intensity of tactile and visual stimuli is represented in single neurons of the primate PFC alongside their perceived intensity, i.e., the animal's subjective experience of a stimulus (de Lafuente and Romo, 2005;Merten andNieder, 2012, 2013).…”

Neuronal Reward and Decision Signals: From Theories to Data

“…They become apparent when decoupling the decision temporally or spatially from the subsequent reporting action. The signals occur without, separately from, or stronger than object or action signals in prefrontal, premotor, secondary somatosensory, and anterior cingulate cortex with vibrotactile stimulus comparisons (FIGURE 42A) (212,312,334,340,489,490) and visual stimulus detection (360,361). They are also seen as buildup activity in supplementary eye fields and superior colliculus during visual search (587) and random dot motion discrimination (230).…”