Saturday, June 30, 2007

Captain My Captain


O Captain! my Captain! our fearful trip is done;
The ship has weathered every rack, the prize we sought is won;
The port is near, the bells I hear, the people all exulting,
While follow eyes the steady keel, the vessel grim and daring.
But O heart! heart! heart!
O the bleeding drops of red!
Where on the deck my Captain lies,
Fallen cold and dead.
Brain's voluntary chain-of-command ruled by not one but two captains
By Michael Purdy

June 18, 2007 -- A probe of the upper echelons of the human brain's chain-of-command has found strong evidence that there are not one but two complementary commanders in charge of the brain, according to neuroscientists at Washington University School of Medicine in St. Louis.

It's as if Captains James T. Kirk and Jean-Luc Picard were both on the bridge and in command of the same starship Enterprise.


In reality, these two captains are networks of brain regions that do not consult each other but still work toward a common purpose — control of voluntary, goal-oriented behavior. This includes a vast range of activities from reading a word to searching for a star to singing a song, but likely does not include involuntary behaviors such as control of the pulse rate or digestion.
So there you have it. The captains don't talk to each other. This article (of course) is in reference to the paper by Dosenbach and colleagues (2007),1 in which they described two distinct task-control networks:
A frontoparietal network included the dorsolateral prefrontal cortex and intraparietal sulcus. This network emphasized start-cue and error-related activity and may initiate and adapt control on a trial-by-trial basis. The second network included dorsal anterior cingulate/medial superior frontal cortex, anterior insula/frontal operculum, and anterior prefrontal cortex. Among other signals, these regions showed activity sustained across the entire task epoch, suggesting that this network may control goal-directed behavior through the stable maintenance of task sets.

Scientists exploring the upper reaches of the brain's command hierarchy were astonished to find not one but two brain networks in charge, represented by the differently-colored spheres on the brain image above. ... The regions in each network talked to each other often but never talked to brain regions in the other network. [from the wustl "two captains" news release by M. Purdy]

Shouldn't they be talking to each other at some point?
These two independent networks appear to operate on different time scales and affect downstream processing via dissociable mechanisms. [from Dosenbach et al., 2007]
If they're not talking directly to each other2, how does the sustained control network communicate the need to adjust performance on a moment-to-moment basis, and how does making a mistake (for instance) engage the sustained control network?

For possible answers to those questions, one is drawn to a popular model of discrete regions for cognitive control3 and conflict monitoring (Botvinick et al., 2001), which has been discussed at Developing Intelligence. Interestingly, Botvinick and colleagues seem to have located the areas for errors/trial adjustments and the areas for sustained task performance in the opposite structures from Dosenbach et al. (2007) [...sort of]. Namely, the conflict monitoring hypothesis (see also Botvinick et al., 2004; Yeung et al., 2004) places "watching out for response conflicts" (e.g., naming the ink color here -- BLUE -- as in the Stroop task) and "watching out response gaffes" (e.g., saying "blue" instead of "red" to the word above) in the anterior cingulate cortex. These functions would be part of the frontoparietal network for Dosenbach et al. (2007). Meanwhile, for Botvinick et al., the dorsolateral prefrontal cortex (PFC) implements "control"4 on a trial-by-trial basis and maintains task set on a sustained basis. Similarly, as part of the frontoparietal network, the dorsolateral PFC is involved in implementing adaptive control on a trial-by-trial basis for Dosenbach et al. In the longer run, however, this latter scheme puts another network (anterior cingulate/frontal operculum/anterior PFC) in charge of maintaining task set.

How do these views relate to other recent studies that emphasize the brain's network properties? As reviewed in the June 15 PERSPECTIVES in Science, Neural Networks Debunk Phrenology:
The studies show that network interactions among anatomically discrete brain regions underlie cognitive processing and dispel any phrenological notion that a given innate mental faculty is based solely in just one part of the brain.
Does anyone really believe in phrenology any more? Who advocates such a view? Cognitive neuropsychologists? Single-unit neurophysiologists? OR has localization of function in discrete networks (rather than an individual structure or a bump on the head) become the new phrenology? I think the story goes like this: complex adaptive behavior is an emergent property of network interactions. This is certainly not a new idea (see any number of publications by Joaquin Fuster), as stated in a prior post by The Neurocritic:
In contrast to the outdated (Fuster, 2000) Modular Paradigm (in which cognitive functions and the contents of cognition are localized in discrete regions [discrete networks??] dedicated to the specific functions and domains), Fuster has long supported the Network Paradigm where higher cortical functions are distributed across brain regions, showing extensive intersection and overlap. In this scheme, one neuron can be part of many networks.
Fuster's unique twist is his emphasis on "extensive intersection and overlap," particularly at the highest levels of the hierarchy [where things are most distributed, rather than orchestrated by a single "central executive"].

To be fair, novel approaches by the non-Fuster investigators (reviewed by Knight in the Debunking Phrenology commentary) include characterizing the nature of neuronal oscillations that synchronize activity across cortical regions [but even aspects of that research are not all that new, of course; the recent Science article by Womelsdorf, Singer et al. certainly builds on their prior work dating back to the late 80's-early 90's].

At the end of the day, however, a lot of time and effort and money is still spent in search of the captain(s).


Footnotes

1 See also The New Neuroscience Party Game.

2 But see this quote on page 11077: "The frontoparietal and cinguloopercular control networks were strongly intraconnected and quite separate from each other, suggesting that they carry out dissociable control functions. The networks may nonetheless communicate with each other."

3 The function formerly known as "executive control."

4 It would be good to listen to The Faint's The Conductor (Thin White Duke Mix), but I couldn't find the mp3 online. Imagine "control control control control control control..." repeated 100 times to an electroclash beat. Other tracks available here, though.


References

Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD. (2001). Conflict monitoring and cognitive control. Psychol Rev. 108:624-52.

Botvinick MM, Cohen JD, Carter CS. (2004). Conflict monitoring and anterior cingulate cortex: an update. Trends Cog Sci. 8:539-46.

Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE. (2007). Distinct brain networks for adaptive and stable task control in humans. PNAS 2007 Jun 18; [Epub ahead of print].

Fuster JM (2000). The module: crisis of a paradigm (book review, The New Cognitive Neurosciences Second Edition, M.S. Gazzaniga, Editor-in-Chief, MIT Press). Neuron 26:51-53.

Knight RT. (2007). Neural networks debunk phrenology. Science 316:1578-9.

Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P. (2007). Modulation of neuronal interactions through neuronal synchronization. Science 316:1609-12.

Yeung N, Cohen JD, Botvinick MM. (2004). The neural basis of error detection: conflict monitoring and the error-related negativity. Psychol Rev. 111:931-59.

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