Right inferior frontal cortex: addressing the rebuttals

We recently provided an updated theory of the role of posterior ventral right inferior frontal cortex (hereafter rIFC) in inhibitory response control (Aron et al., 2014). We claimed that when rIFC is triggered by a stop signal, unexpected event or endogenous rule, it engages a brake; i.e., it slows, pauses, or completely stops an action via one or more rIFC-based fronto-basal-ganglia networks. This account was challenged by two recent papers: “Ten years of inhibition revisited” by Swick and Chatham (2014), and “A functional network perspective on response inhibition and attentional control” by Erika-Florence et al. (2014). Here we address the points made in those papers. Swick and Chatham (hereafter S&C) argue that rIFC instead monitors for cues that signal a change of action, and question our interpretation of Chatham et al. (2012). In that study, for the stop signal task, subjects tried to stop when a signal occurred; in the double Go task, when the signal occurred, subjects continued their response and then repeated it. Right IFC was activated both for stop and double Go trials. However, the signal on double Go trials slowed the primary response, consistent with infrequent events recruiting a brake. S&C further showed that double Go trials without primary task slowing also activated the rIFC. But such activation could still reflect a brake that fails to slow the response. S&C ask: (a) Why should braking occur on such trials when they are contrary to task goals (to respond quickly)? We propose, along with others (Chatham et al., 2012; Wiecki and Frank, 2013), that braking, at least of the externally triggered, rather than endogenously triggered variety, is inextricably linked with salience detection—at least when salient signals are relevant to ongoing behavior (also see Wessel and Aron, 2014). (b) How can we argue that the above rIFC activation reflected “braking” when it was too late to affect behavior, when, at the same time, it has been shown that rIFC BOLD correlates with SSRT (Whelan et al., 2012)? We see no contradiction here. Right IFC activation within a subject could be similar for double Go trials (slowed or not) and stop trials (successful or not)—reflecting triggering of rIFC. On the other hand, rIFC activation between-subjects varies for successful stop trials, with several studies showing increased activation for faster stop speeds (Aron and Poldrack, 2006; Congdon et al., 2010; Whelan et al., 2012; Cai et al., 2014). (c) Why is rIFC more strongly recruited on double Go trials than during the stop task itself? That comparison is confounded by the double Go condition always being performed first. Activation decreases with practice (Kelly and Garavan, 2005) although withinsession practice effects specifically for response inhibition paradigms have not, to our knowledge, been reported. (d) Why is rIFC recruitment sustained even when subjects must always produce a “go” response and proactive inhibitory control is unnecessary? Activation for the contrast of double Go vs. rest blocks covered almost the entire right frontal lobe, making interpretation difficult in relation to braking. Using ECoG we showed rIFC activation even when a stop signal did not occur (but was merely expected), and that the time of activation was around the response and not the anticipated time of the stop signal (Swann et al., 2013). S&C correctly observe that the tight timing to the response only occurred in 2 out of 5 patients. However, we then showed (Wessel et al., 2013) that rIFC direct electrical stimulation (DES) just before the response induced slowing in a braking context. S&C argue this could arise from non-specific effects of DES (mentioning that frontal DES at 60Hz induces visual hallucinations). But note: (i) our frontal effect occurred relative to a control site, using two brief pulses of DES (not the 60Hz method, nor the “short train” method of 5 pulses, with 3ms interpulse interval, Axelson et al., 2009) (ii) it was context-specific—slowing only those subjects who were not already slowing, (iii) it more strongly affected trials on which braking was needed, and (iv) DES like ours can have highly specific effects (Desmurget et al., 2013). It could be argued that such rIFC recruitment reflects a kind of monitor (Chatham et al., 2012; Chevalier et al., 2014) that activates in proximity to the irrevocable/ballistic stage of an action, so long as that action is contingent on the absence of some countermanding signal. However, it is unclear how disrupting the activity of this putative monitor would elongate RT unless response initiation has to wait until the monitor function is complete; yet other work has shown that responses are initiated as early as 200ms after the go stimulus (Jahfari et al., 2010). For us, the data are most compatible with rIFC being part of a brake. S&C question the anatomical specificity of our ECoG studies to rIFC. While