Frontal Cortex and the Hierarchical Control of Behavior

Abstract

The frontal lobes are important for cognitive control, yet their functional organization remains controversial. An influential class of theory proposes that the frontal lobes are organized along their rostrocaudal axis to support hierarchical cognitive control. Here, we take an updated look at the literature on hierarchical control, with particular focus on the functional organization of lateral frontal cortex. Our review of the evidence supports neither a unitary model of lateral frontal function nor a unidimensional abstraction gradient. Rather, separate frontal networks interact via local and global hierarchical structure to support diverse task demands.

Keywords: cognitive control; executive function; frontal lobes.

Figure I

Architectures for hierarchical control. (A) Schematic of the simple model of the Stroop task from [91]. Thick lines depict stronger connection strength. (B) Task schematic and rule structure for a hierarchical control task. A unitary context “hub” (C) and a hierarchical control architecture (D) could both solve this problem, though with different strengths and weaknesses.

Figure II

Schematic of elaboration of the cortico-striatal model for hierarchical control. Details of the cortico-striatal loops are simplified to emphasize the nested looping structure. Each loop regulates a separate region of frontal cortex. Striatal components of each lower orderloop receive top down context information from higher order areas of FC through diagonal connections (red arrows).

Figure III

Model schematics showing top-down versus feedback processing in the medial-lateral hierarchical architecture from [97].

Figure 1

Hierarchical control demands affecting rostro-caudal activation. (A) Policy abstraction can be operationalized in terms of the depth of decision tree relating contexts to actions. Here, the presence of a parent contextualizes the relation between the environment and speech volume. (B) Temporal abstraction (red curved arrow) refers to contextual representations that are sustained over time and/or abstract over intervening episodes or subtasks. Here, the goal of “take shower” abstracts over several subtasks en route to the goal of being clean. When a temporally abstract context is used to guide control of lower order tasks, rather than information available in the stimulus, this is referred to as episodic control (brown curved arrows). Thus, if prior steps or the overall structure of a shower plan is referenced to determine what subtask to perform, this is episodic control.

Figure 2

The three zones of rostro-caudal lateral frontal organization. (A) The approximate location of anatomical labels defined in the text on an inflated lateral surface. Dorsal prePM (prePMd) and ventral prePM (prePMv) are separately labeled. (B) Small shapes plot locations of peak foci on the lateral surface from studies that located differences in two or more levels of abstraction. Color distinguishes the three functional zones. Small green spheres plot sensory-motor control (or first order policy). Yellow shapes plot studies manipulating contextual control. Yellow spheres involve 2^nd order control. Studies using third order policy are diamonds. Maroon shapes plot studies manipulating schematic control regardless of policy level. Large shapes plot means. The mean sensory motor (Green Sphere: Y=−7) was most caudal. Within the mid-lateral contextual control zone, second and third order control without schematic control demands differed from rostral (third order Yellow Diamond: Y=26) to caudal (second order Yellow Sphere: Y=15). However, regardless of policy, schematic control demands shifted things to most rostral (Maroon sphere: Y=49). (C) The 17-network parcellation of resting state from [76]. Colors highlight the networks that roughly corresponds with the three functional zones: Schematic (Maroon), Contextual (Yellow), and Sensory-Motor (Green).

Figure 3

Gating refers to input and output from working memory. (Top) Updating information into working memory is input gating. Selecting information from within working memory to guide action is output gating. (Bottom) A second order rule from [37] uses a higher order context (number) to decide which lower order context (letter or wingding) is used in a final match decision (red box indicates correct response). The order of second and first order contexts determines gating demands. When a second order context comes first, the relevant first order context can be input gated. When it comes last, the first order context must be output gated from working memory.

Figure 4

Schematic summary of the functional relationships among regions of frontal cortex. Regions within the schematic (maroon), contextual (yellow), and sensory-motor (green) control zones are labeled along with their respective influences. Heavy, solid black arrows show primary direction of influence, based on structural and effective connectivity. Dashed black arrows show weaker influences. Colored arrows show task-dependent domain specific influences. The architecture features both global and local hierarchical relations, with the contextual control zone influencing the other zones, and then further local hierarchy within the contextual and sensory-motor zones. Individual regions also differ in domain specificity or proximity to different domain influences.