Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex

Abstract

Everyday circumstances require efficient updating of behavior. Brain systems in the right inferior frontal cortex have been identified as critical for some aspects of behavioral updating, such as stopping actions. However, the precise role of these neural systems is controversial. Here we examined how the inferior frontal cortex updates behavior by combining reversible cortical interference (transcranial magnetic stimulation) with an experimental task that measures different types of updating. We found that the right inferior frontal cortex can be functionally segregated into two subregions: a dorsal region, which is critical for visual detection of changes in the environment, and a ventral region, which updates the corresponding action plan. This dissociation reconciles competing accounts of prefrontal organization and casts light on the neural architecture of human cognitive control.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Typical trial sequence illustrating the different trial types in the three contexts and the required responses. The color-response mapping was counterbalanced across subjects. On signal trials, the colored cue turned bold for 250 ms after a variable delay (SOA). On signal-ignore and dual-signal trials, SOAs were fixed (100, 250, or 400 ms); on stop-signal trials, SOA was dynamically adjusted (Materials and Methods). Time intervals for signal and no-signal trials are in milliseconds. Presumed control processes for dual- and stop-signal trials are indicated in gray.

Fig. 2.

At short delays (SOA; Upper), the decision stage for task 2 is postponed until the decision stage for task 1 is finished (indicated by the vertical black line). This creates a bottleneck period. At longer SOAs (Lower), the decision stage of task 1 is completed when the perceptual-processing stage of task 2 is finished. Therefore, the decision stage of task 2 can start immediately at longer SOAs.

Fig. 3.

(A) At short SOAs (Upper), prolongation of the perceptual stage of task 2 is absorbed within the bottleneck period. At longer SOAs (Lower) there is no bottleneck, so the prolongation of the perceptual stage of task 2 should be detected. Consequently, interfering with prebottleneck processes such as visual detection should produce a RT deficit that increases with SOA. (B) Prolongation of stages at or after the bottleneck should be detected both at short (Upper) and long (Lower) SOAs. Consequently, interfering with processes at or after the bottleneck, such as action updating, should produce a uniform RT deficit that does not depend on SOA.

Fig. 4.

Cortical regions that were disrupted with continuous theta-burst stimulation. Right inferior frontal gyrus (rIFG), right inferior frontal junction (rIFJ), and presupplementary motor area (preSMA) shown in one participant. All sites were defined from individual neuroanatomical landmarks (Materials and Methods) (1) rIFG, (2) rIFJ, and (3) preSMA. Sulci: red, lateral sulcus; green, precentral sulcus; dark blue, inferior frontal sulcus; magenta, cingulate sulcus; light blue, dorsal cingulate branch.

Fig. 5.

Data of the linear mixed model for the baseline (Sham) condition. (A) A goRT difference between the three contexts [F(2, 1006) = 433.3, P < 0.001]. goRTs were slower in the stop context than in the dual-task context and ignore context (t = 20.2, P < 0.001, and t = 28.6, P < 0.001, respectively). In addition, goRTs were longer in the dual-task context than in the ignore context (t = 8.3, P < 0.001). (B) The dual-response latency substantially decreased when SOA increased [F(2,1006) = 1267.8, P < 0.0001]. There was also a smaller effect of SOA on the latency of the first response on dual-signal trials [F(2,1006) = 39.202, P < 0.0001].

Fig. 6.

Results of linear mixed effect analyses. Error rates were minimal (SI Text). Disruption of rIFG and rIFJ increased the stop latency (SSRT) and the dual-response latency (DRT2) (A and B). By contrast, goRT and the latency of the first response on dual-signal trials (DRT1) decreased. Crucially, the roles of rIFG and rIFJ were dissociated by the SOA analysis: the effect of stimulation for DRT2 depended on SOA for rIFJ, but not for rIFG (C). The interaction between site and SOA was significant (SI Text). Finally, stimulation of preSMA did not reliably influence signal performance (D). Asterisks indicate that the LME contrast with baseline (Sham) condition was significant (α = 0.05; black asterisks indicate site-specific effects; gray asterisks indicate site-nonspecific effects). Error bars indicate ±1 SEM of the LME estimates.