Human anterior cingulate neurons and the integration of monetary reward with motor responses

Abstract

The human dorsal anterior cingulate cortex (dACC) has been implicated in cognitive processes that have been proposed to play a role in integrating contextual information needed to select or modify appropriate motor responses. In humans, however, there has been little direct evidence tying the dACC to the integration of contextual information and behavioral response. We used single-neuron recordings from human subjects to evaluate the role of the dACC in reward-based decision making. Subjects undergoing planned surgical cingulotomy performed a task where they were instructed to make specific movements in response to changing monetary rewards. In many neurons, activity increased in response to a diminished reward, and was also predictive of the movement ultimately made. After dACC ablation, subjects made selectively more errors when they were required to change movement based on reward reduction. These findings suggest that the dACC in humans plays an important role in linking reward-related information with alternative actions.

Neural dynamics of error processing in medial frontal cortex

“…Overall, these results are consistent with a series of recent studies showing that portions of the general region labeled Fcingulate cortex_ are involved in action selection based on the expected outcome of an action (Bush et al, 2002;Hadland et al, 2003;Shima and Tanji, 1998), integrating information regarding a motor response and its potential outcome (Williams et al, 2004). Our results illustrate how a specific portion of the medial frontal cortex, the RCZa, might receive evaluative information, which can be used to adapt behavior accordingly (Holroyd et al, 2004a;Ridderinkhof et al, 2004).…”

Neural substrates of choice selection in adults and adolescents: Development of the ventrolateral prefrontal and anterior cingulate cortices

“…The current results show activation in the dorsal ACC. This is consistent with a previous study using the same task (Ernst et al, 2004), and with single-unit recordings in humans demonstrating the dorsal ACC's role in linking reward information with appropriate actions (Williams et al, 2004). The dorsal ACC activation suggests that the wheel of fortune task taxes cognitive capacity, particularly the ability to resolve conflicts to take action, rather than the emotional processing of stimulus salience.…”

“…The ventral division (BA 24,25,32,33), on the other hand, is considered to be the "affective" ACC, and is predominantly involved in the representation of the emotional salience of stimuli (Phillips, Drevets, Rauch, Lane, 2003). Previous work has shown engagement of both regions in studies of reward-related processes (e.g., Cohen, Heller, Ranganath, 2005;Rogers, Ramnani, Mackay, Wilson, Jezzard, Carter, Smith, 2004) and the selection of options (e.g., Ernst et al, 2004;Williams, Bush, Rauch, Cosgrove, Eskandar, 2004;Hadland, Rushworth, Gaffan, Passingham, 2003). The current results show activation in the dorsal ACC.…”

“…Neuropsychological, lesion, and functional neuroimaging studies in humans have identified the OFC/VLPFC (Arana et al, 2003;Elliott et al, 1999;Ernst et al, 2002;Paulus et al, 2001;Rogers et al, 1999;Walton et al, 2004;Rushworth, Buckley, Gough, Alexander, Kyriazis, McDonald, Passingham, 2005;Elliott, Rees, Dolan, 1999) and ACC (Bush et al, 2002;Ernst et al, 2004;Rogers et al, 2004;Walton et al, 2004;Williams et al, 2004) as key neural substrates of decision-making processes. Often modulated by both risk (Critchley et al, 2001;Cohen et al, 2005) and reward (Rogers et al, 2004), these structures are purported to support specific functions that are specialized by subregions (e.g., lateral vs. medial OFC, dorsal vs. ventral ACC).…”

Dissociable Contributions of Anterior Cingulate Cortex and Basolateral Amygdala on a Rodent Cost/Benefit Decision-Making Task of Cognitive Effort

“…Patients with damage to either region demonstrate impairments on laboratory models of 'real-world' decision making where levels of reward and cost are varied across options (Bechara et al, 1999;Brand et al, 2007;Manes et al, 2002;van Honk et al, 2013). Similarly, functional neuroimaging and intracranial electrophysiology suggest that the amygdala and ACC are involved in evaluating costs and rewards to guide subsequent behavior (Basten et al, 2010;Jenison et al, 2011;Smith et al, 2009;Williams et al, 2004), and internally generated changes in choice correlate with amygdala and ACC activity (Sokol-Hessner et al, 2013;Walton et al, 2004).…”