The Subthalamic Nucleus Contributes to Post-error Slowing James F. Cavanagh 1,2 , Joseph L. Sanguinetti 3 , John J. B. Allen 3 , Scott J. Sherman 3 , and Michael J. Frank 2 Abstract ■ pFC is proposed to implement cognitive control via di- rected “top–down” influence over behavior. But how is this feat achieved? The virtue of such a descriptive model is contingent on a mechanistic understanding of how motor execution is altered in specific circumstances. In this report, we provide evidence that the well-known phenomenon of slowed RTs fol- lowing mistakes (post-error slowing) is directly influenced by the degree of subthalamic nucleus (STN) activity. The STN is proposed to act as a brake on motor execution following con- flict or errors, buying time so a more cautious response can be made on the next trial. STN local field potentials from nine Parkinson disease patients undergoing deep brain stimulation surgery were recorded while they performed a response con- flict task. In a 2.5- to 5-Hz frequency range previously associated with conflict and error processing, the degree phase consistency preceding the response was associated with increasingly slower RTs specifically following errors. These findings provide compel- ling evidence that post-error slowing is in part mediated by a corticosubthalamic “hyperdirect” pathway for increased response caution. ■ INTRODUCTION As our understanding of the nature of cognitive and execu- tive control grows, increasingly fine-tuned descriptions of these processes have begun to emerge (Rushworth, Noonan, Boorman, Walton, & Behrens, 2011; Buckley et al., 2009; Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004). It is widely believed that one means of imple- menting control involves directed “top–down” influence over prepotent or habitual actions, especially in difficult situations (Miller & Cohen, 2001). Although this descrip- tive model is helpful, much work remains to be done to explain the distinct neural mechanisms by which such top–down control alters action selection. In this re- port, we provide evidence that the subthalamic nucleus (STN) contributes to the degree of RT slowing following an error. Extensive evidence implicates the pFC in the realization of an error (Gehring, Liu, Orr, & Carp, 2012; Botvinick, Braver, Barch, Carter, & Cohen, 2001; Carter et al., 1998), yet the mechanistic details of how erroneous per- formance is resolved are less well specified. Post-error RT slowing is a well-known feature in cognitive accounts of performance monitoring (Botvinick et al., 2001; Gehring & Fencsik, 2001; Rabbitt, 1966), whereupon the response following an error is slower and more accurate than the average response (Luce, 1986; Laming, 1979). The covary- ing combination of slowed responses and increased accu- racy is best represented by a single latent construct in formal models of performance: an increased decision threshold (Ratcliff & McKoon, 2008; Luce, 1986). An increased decision threshold thus accounts for a shift in the speed–accuracy tradeoff toward increased response caution. One candidate neural system—the hyperdirect cortico-STN pathway—has been proposed to specifically act to increase decision threshold following signals of the need for control (Ratcliff & Frank, 2012; Cavanagh et al., 2011; Frank, 2006). The STN are small subcortical nuclei that lie between the brainstem and pallidum. Long considered a part of the corticostriatal indirect pathway, they have been im- plicated as a part of an inhibitory system that prevents motor gating, acting in antagonism to the facilitatory direct pathway (Mink, 1996; Alexander & Crutcher, 1990). The existence of a distinct extrastriatal hyperdirect infor- mation processing stream has been supported by recent descriptions of the cortico-BG system including histologi- cal (Haynes & Haber, 2013; Nambu, Tokuno, & Takada, 2002; Nambu, Tokuno, & Hamada, 2000), functional imaging (Mansfield, Karayanidis, Jamadar, Heathcote, & Forstmann, 2011; Aron & Poldrack, 2006), functional con- nectivity (Forstmann et al., 2012; Aron, Behrens, Smith, Frank, & Poldrack, 2007), electrophysiological (Zaghloul et al., 2012; Cavanagh et al., 2011), and computational (Wiecki & Frank, 2013; Ratcliff & Frank, 2012; Frank, 2006) evidence. In the hyperdirect pathway, motor cortex and premotor cortex bypass the striatum and project 1 University of New Mexico, 2 Brown University, 3 University of Arizona © 2014 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 26:11, pp. 2637–2644 doi:10.1162/jocn_a_00659