Relation of ordinal position signals to the expectation of reward and passage of time in four areas of the macaque frontal cortex

Abstract

Berdyyeva TK, Olson CR. Relation of ordinal position signals to the expectation of reward and passage of time in four areas of the macaque frontal cortex. J Neurophysiol 105: 2547-2559, 2011. First published March 9, 2011 doi:10.1152/jn.00903.2010.-Neurons in several areas of the monkey frontal cortex exhibit rank selectivity, firing differentially as a function of the stage attained during the performance of a serial order task. The activity of these neurons is commonly thought to represent ordinal position within the trial. However, they might also be sensitive to factors correlated with ordinal position including time elapsed during the trial (which is greater for each successive stage) and the degree of anticipation of reward (which probably increases at each successive stage). To compare the influences of these factors, we monitored neuronal activity in the supplementary motor area (SMA), presupplementary motor area (pre-SMA), supplementary eye field (SEF), and dorsolateral prefrontal cortex during the performance of a serial order task (requiring a series of saccades in three specified directions), a variable reward task (in which a cue displayed early in the trial indicated whether the reward received at the end of the trial would be large or small), and a long delay task (in which the monkey had simply to maintain fixation during a period of time approximating the duration of an average trial in the serial order task). We found that rank signals were partially correlated with sensitivity to elapsed time and anticipated reward. The connection to elapsed time was strongest in the pre-SMA. The connection to anticipated reward was most pronounced in the SMA and SEF. However, critically, these factors could not fully explain rank selectivity in any of the areas tested. monkey; neuronal activity; serial order TO BE ABLE TO PERFORM a series of actions in the correct order requires that neurons somewhere in the brain keep track of the sequence of events. Neurons that systematically change their firing rate according to ordinal position within a serial order task are prominent candidates for this role. Such neurons had been often reported in frontal cortical areas including the supplementary motor area (SMA) (Berdyyeva and Olson 2010;

A comparison of neural responses to appetitive and aversive stimuli in humans and other mammals

“…However, as no studies used aversive and appetitive stimuli together, the relative proportion or exact nature of activity is currently unclear. While limited evidence suggests that both GABA and glutamate within the Cg/M2 regions are involved in mediating aversion-related processing, particularly related to pain and fear (Albrechet-Souza et al, 2009Wang et al, 2005Wang et al, , 2008, non-GABAergic cells within these regions also respond during reward anticipation linked to action selection and effort (Berdyyeva and Olson, 2011;Hillman and Bilkey, 2012;Sul et al, 2011).…”

Davida Teller Award Lecture 2013: The importance of prediction and anticipation in the control of smooth pursuit eye movements

“…In addition, neurons within SEF show firing patterns that correlate with the onset time and the direction of anticipatory smooth eye movements (de Hemptinne et al, 2008). SEF would appear to be a good candidate for integrating sensory motion with expected motion because it receives signals from motion centers, such as the medial superior temporal area (MST), and it plays a role in high-level decisions associated with the planning of saccades (Schall, Stuphorn, & Brown, 2002;Yang, Hwang, Ford, & Heinen, 2010;Berdyyeva & Olson, 2011).…”

Sources of bias and uncertainty in a visual temporal individuation task

“…There exist neurons in a variety of premotor areas-most notably, the basal ganglia and frontal cortex-that appear to be rank-orderselective (ROS) neurons; that is, they change systematically their firing rate depending on the serial order position of an action within a sequence (Tanji, 2001). Prefrontal ROS neurons appear to code rank order independently of passage of time (Berdyyeva & Olson, 2011) and, crucially, also appear to be rank-order generalists; that is, they seem to signal temporal ordinal position for both action and object sequences (Berdyyeva & Olson, 2009. As such, the most recent investigations in this field seem to suggest that frontal ROS neurons may be implicated generally in tasks requiring temporal serial order judgments, including action, memory, and perception.…”