Can signals from the prefrontal cortex alone trigger a readiness potential in the pre-supplementary motor area?

Question

Background

In Haggard, Patrick. "Human volition: towards a neuroscience of will." Nature Reviews Neuroscience 9.12 (2008): 934., the author states in the caption of Figure 1 (pg. 4):

The primary motor cortex (M1) receives two broad classes of inputs. One key input (left-hand panel) reaches M1 from the supplementary motor area (SMA) and the pre-supplementary motor area (preSMA), which in turn receives inputs from the basal ganglia and the prefrontal cortex.

Question

I'm failing to disambiguate the ending phrase (emphasis mine)

basal ganglia and the prefrontal cortex

Is the "and" meant to be interpreted as a logical AND or logical OR? In other words, does a readiness potential in the pre-supplementary motor area (preSMA) require an active input from both the basal ganglia AND the prefrontal cortex concurrently or is a sufficiently strong signal from either region alone sufficient?

Hunch

My guess is that the latter is the case. For example, on the very same caption of Figure 1 part b, the author indicates that the signal from the frontopolar cortex starts a chain that ends with voluntary action of the right hand. This indicates that executive control from the frontopolar cortex alone can trigger an eventual movement. Since this is only a hunch, I still want to clarify the point of confusion.

Intent

I'm asking this question because I want to figure out a situation at the behavioral level, namely if people can trigger movements purely by executive function and independently of primal urges/apprehensions.

Standards

It may be difficult to give a direct and bulletproof answer to the question without a deliberate experiment (see comment). However, I find it acceptable to have a lower standard for potential answer post - for example, conjectures based on indirect evidence.

Answer 1

The original author is not making a claim one way or another for logical AND or logical OR within this context. The statement

the pre-supplementary motor area (preSMA), which in turn receives inputs from the basal ganglia and the prefrontal cortex

is referring only to inputs to the preSMA; it is not making any strong statements about which inputs are causal for the readiness potential, only mentioning that those connections exist and therefore could be involved in communication of the readiness potential.

There are in fact cortico-cortical loops that route through the basal ganglia (see for example Lopez-Paniagua & Seger, 2011; there is probably a better canonical reference but not one I have in hand right now); if there is a signal from frontopolar cortex that reaches motor cortex that does not tell you the basal ganglia were not involved. A signal originating in cortex could communicate with another cortical area both via direct cortico-cortico and via basal ganglia open loops, not that a basal ganglia signal preceded both.

The only way to truly answer your title question would be to somehow inactivate either basal ganglia or PFC inputs to preSMA. I am not aware of such an experiment, it would be quite technically and ethically difficult both in humans and primates, and PFC is less developed in rodents so it's difficult to make direct analogy there.

More generally, the basal ganglia are definitely involved in voluntary movement. One can simply observe Parkinsonian patients, who have difficulties initiating voluntary movements due to basal ganglia pathology (DeLong 1990 discusses some of the motor impacts of lesions of the basal ganglia).

If you want to know whether movements can be triggered "purely by executive function and independently of primal urges/apprehensions" you will not find the answer simply by identifying whether the basal ganglia are involved or not. Although yes, the basal ganglia are often associate with more "primal" actions, that is only relevant in the absence of neocortex. In the presence of neocortex, that organization no longer applies because cortex influences the basal ganglia (and vice versa).

Furthermore, it does not seem possible to separate out the basal ganglia from neocortex in terms of cognitive control networks (Duncan 2010, Cole et al 2013), since coactivation of those areas is typically observed and not dissociable.

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Cole, M. W., Laurent, P., & Stocco, A. (2013). Rapid instructed task learning: A new window into the human brain’s unique capacity for flexible cognitive control. Cognitive, Affective, & Behavioral Neuroscience, 13(1), 1-22.

DeLong, M. R. (1990). Primate models of movement disorders of basal ganglia origin. Trends in neurosciences, 13(7), 281-285.

Duncan, J. (2010). The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends in cognitive sciences, 14(4), 172-179.

Lopez-Paniagua, D., & Seger, C. A. (2011). Interactions within and between corticostriatal loops during component processes of category learning. Journal of cognitive neuroscience, 23(10), 3068-3083.