Stability or Plasticity? - A Hierarchical Allostatic Regulation Model of Medial Prefrontal Cortex Function for Social Valuation

Abstract

The medial prefrontal cortex (mPFC) has long been recognized as the key component of the neurocircuitry involved in various social as well as non-social behaviors, however, little is known regarding the organizing principle of distinctive subregions in the mPFC that integrates a wide range of mPFC functions. The present study proposes a hierarchical model of mPFC functionality, where three functionally dissociable subregions, namely, the ventromedial prefrontal cortex (vmPFC), rostromedial prefrontal cortex (rmPFC), and dorsomedial prefrontal cortex (dmPFC), are differentially involved in computing values of decision-making. According to this model, the mPFC subregions interact with each other in such a way that more dorsal regions utilize additional external sensory information from environment to predict and prevent conflicts occurring in more ventral regions tuned to internal bodily signals, thereby exerting the hierarchically organized allostatic regulatory control over homeostatic reflexes. This model also emphasizes the role of the thalamic reticular nucleus (TRN) in arbitrating the transitions between different thalamo-cortical loops, detecting conflicts between competing options for decision-making, and in shifting flexibly between decision modes. The hierarchical architecture of the mPFC working in conjunction with the TRN may play a key role in adjusting the internal (bodily) needs to suit the constraints of external (environmental) variables better, thus effectively addressing the stability-plasticity dilemma.

Keywords: allostasis; decision-making; insula; interoception; prosociality; self-enhancement; thalamic reticular nucleus.

FIGURE 1

Schematic diagram of anatomical segregation within the medial prefrontal cortex. mPFC can be broadly divided into three functionally and anatomically dissociable subregions: the ventromedial prefrontal cortex (vmPFC) [roughly corresponds to the medial aspect of Brodmann area (BA 11, BA 12, BA 14, and BA 25)], the dorsomedial prefrontal cortex (dmPFC) [BA 9, BA 24 (the pregenual anterior cingulate cortex), and BA 32 (the anterior midcingulate cortex)], and the rostromedial prefrontal cortex (rmPFC) [BA 10, BA 24 (the pregenual anterior cingulate cortex), and BA 32 (the pregenual anterior cingulate cortex)]. The dmPFC and rmPFC are divided by the z-plane of +22, and the rmPFC and vmPFC are divided by the z-plane of –10 (Lieberman et al., 2019). cc, corpus callosum.

FIGURE 2

Functional segregation of mPFC function during ethical consumption under social observation. The rmPFC and the dmPFC encode subject-specific values of purchasing social products (prosocial decision) and non-social products (self-centered decision), respectively, under social observation (context-dependent), whereas the vmPFC encodes subject-specific values of purchasing social products regardless of social observation (context-independent) (Adapted from Jung et al., 2018).

FIGURE 3

The hierarchical allostatic regulation model of mPFC function for social valuation. The mPFC comprises of three functionally dissociable hierarchically organized subregions: the vmPFC, rmPFC, and dmPFC, which are differentially involved in computing values of decision along the ventral-to-dorsal spatial gradient of increasing external sensory inputs (e.g., via the temporal cortex and the parietal cortex) and decreasing internal inputs (e.g., via the brainstem, the hypothalamus, the amygdala, and the nucleus accumbens). The vmPFC computes the internal valuation that generates interoceptive prediction signals and elicits a familiar intuitive response to prevent foreseen bodily imbalance. When two or more mutually incompatible values are simultaneously activated at the level of vmPFC, a conflict (prediction error) may occur triggering the upper levels (i.e., either rmPFC or dmPFC), which would then disengage internal valuation and increase the sensitivity to incoming sensory signals from the external environment to resolve the conflict. Such a process, called external valuation, sends prediction signals to update the preexisting value encoded at the lower level and continues until it finds a new value that resolves the conflict. The newly updated value will be strengthened and internalized through repetition so that it is activated more quickly and easily in similar situations later without causing a conflict.

FIGURE 4

Role of the thalamic reticular nucleus (TRN) in shifting between the thalamo-cortical loops. Mutually inhibiting interneurons densely distributed in the TRN are perfectly suited for detecting conflicts between non-compatible units being engaged simultaneously, which can lead to disinhibition of other non-occupied units in the external sector, resulting in an attentional shift between different thalamo-cortical loops. In this diagram, simultaneous activation of two mutually competitive units (i.e., A and B) in the internal sector would lead to a sector-wide disinhibition of the thalamic projection neurons (i.e., C′ and D′) in the external sector, which would then gate the external sector, initiating more elaborated processing of additional external sensory information. Such inhibitory connections are likely to be asymmetrical, that is, favoring the direction from internal to external sectors and therefore prioritizing internal over external valuation. Note that not all the necessary connections are shown for visualization purpose. CTX, cortex; TRN, thalamic reticular nucleus; Thal: thalamus; BF: basal forebrain.