Neural Mechanisms as Putative Targets for Warfighter Resilience and Optimal Performance - Neurotechnology in National Security and Defense - page 56

Second, centrally generated interoceptive states, for example, via contextual asso-
ciations from memory, reach the insular cortex via temporal and parietal cortex to
generate body states based on conditioned associations (Gray and Critchley 2007).
Third, within the insular cortex, there is a dorsal-posterior to inferior-anterior orga-
nization from granular to agranular, which provides an increasingly “contextual-
ized” representation of the interoceptive states (Shipp 2005), irrespective of whether
it is generated internally or via the periphery. These interoceptive states are made
available to the orbitofrontal cortex for context-dependent valuation (Kringelbach
2005) and to the ACC for error processing (Carter et al. 1999) and action valuation
(Rushworth and Behrens 2008). Fourth, bidirectional connections to the basolat-
eral amygdala (Reynolds and Zahm 2005) and the striatum (Chikama et al. 1997),
particularly ventral striatum (Fudge et al. 2005), provide the circuitry to calculate
a body prediction error (similar to reward prediction error [Schultz and Dickinson
2000]) and provide a neural signal for salience and learning.
However, body prediction error differences may occur on several levels. For
example, optimal performers may receive different afferent information via the
C-fiber pathway that conveys spatially and time-integrated affective information
(Craig 2007). Alternatively, optimal performers may generate centrally differ-
ent interoceptive states (e.g., via contextual associations from memory), which are
processed in the insular cortex via connections to temporal and parietal cortex to
generate body states based on conditioned associations (Gray and Critchley 2007).
Consistent with this idea, Williamson and colleagues (2002, 2006) suggest that the
neural circuitry underlying central regulation of performance includes the insular
and anterior cingulate cortex that interact with thalamic and brainstem structures
which are important for cardiovascular integration (Williamson et al. 2006) as well
as for the central modulation of cardiovascular responses (Williamson et al. 2002).
Optimal performers may also differentially integrate interoceptive states within the
insular cortex (which shows a clear gradient from the dorsal-posterior to ventral-
anterior part) to provide an increasingly “contextualized” representation of the
interoceptive state (Shipp 2005). This integration may occur irrespective of whether
it is generated internally or via the periphery. The relative increase in activation in
the mid-insula in adventure racers prior to experiencing a breathing load and the
relatively attenuated activation after the load experience support the notion that the
aversive interoceptive experience is less disruptive to these elite athletes compared to
control subjects and may lead to relatively fewer changes in the subjective response
to this stressor. Finally, optimal performers may generate different context-depen-
dent valuation of the interoceptive states within the orbitofrontal cortex (Rolls 2004)
leading to altered error processing in the anterior cingulate (Carter et al. 1998) and
selection of different actions (Rushworth and Behrens 2008). The findings that both
the ventral anterior cingulate and left anterior insula responses are important for the
subjective effects of the breathing load support the notion that optimal performers
may show different integration of aversive interoceptive stimuli. These results are
consistent with those of Hilty and colleagues (2010) who reported that individuals
who perform a handgrip exercise prior to task failure show increased activation in
both the mid/anterior insular cortex and the thalamus. Thus greater activation and
possibly a larger body prediction error might predict suboptimal performance.