Abstract
Background
Based on numerous imaging and electrophysiological studies, the presupplementary motor
area (pre-SMA) and the rostral cingulate motor area are cortical regions considered
to be essential to voluntary movement initiation and behavioral control. However,
their respective roles and functional interactions remain a long-standing and still
debated question.
Methods
Here, we trained 2 rhesus monkeys (Macaca mulatta) in a complex cognitive task to compare the neuronal activity of these 2 regions
on the medial wall during both perceptual and internally guided decisions.
Results
We confirmed the implication of both areas throughout the decision process. Critically,
we demonstrate that instead of a stable invariant role, the pre-SMA and rostral cingulate
motor area manifested a versatile hierarchical relationship depending on the mode
of movement initiation. Whereas pre-SMA neurons were primarily engaged in decisions
based on perceptual information, rostral cingulate motor area neurons preempted the
decision process in case of an internally doubt-driven checking behavior, withholding
pre-SMA recruitment during the time spent inhibiting the habitual action.
Conclusions
We identified a versatile hierarchical organization of the mediofrontal area that
may substantially affect normal and pathological decision processes because adaptive
behaviors, such as doubt-checking and its compulsive counterpart, rely on this subtle
equilibrium in controlling action initiation.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Biological PsychiatryAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Neurophysiology of performance monitoring and adaptive behavior.Physiol Rev. 2014; 94: 35-79
- Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands.Eur J Neurosci. 2002; 15: 887-904
- A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: Neuronal activity during a learned motor task.J Neurophysiol. 1992; 68: 653-662
- Changing directions of forthcoming arm movements: Neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex.J Neurophysiol. 1996; 76: 2327-2342
- Disruption of information processing in the supplementary motor area of the MPTP-treated monkey: A clue to the pathophysiology of akinesia?.Brain. 2003; 126: 95-114
- Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive–compulsive disorder.Arch Gen Psychiatry. 2004; 61: 564-576
- Error-related hyperactivity of the anterior cingulate cortex in obsessive–compulsive disorder.Biol Psychiatry. 2005; 57: 287-294
- Action monitoring and medial frontal cortex: Leading role of supplementary motor area.Science. 2014; 343: 888-891
- The role of the medial frontal cortex in cognitive control.Science. 2004; 306: 443-447
- Conflict monitoring versus selection-for-action in anterior cingulate cortex.Nature. 1999; 402: 179-181
- Pre-SMA actively engages in conflict processing in human: A combined study of epicortical ERPs and direct cortical stimulation.Neuropsychologia. 2013; 51: 1011-1017
- Anterior cingulate conflict monitoring and adjustments in control.Science. 2004; 303: 1023-1026
- Neurons in the cingulate motor area signal context-based and outcome-based volitional selection of action.Exp Brain Res. 2013; 229: 407-417
- Organization of prefrontal outflow toward frontal motor-related areas in macaque monkeys.Eur J Neurosci. 2004; 19: 3328-3342
- Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: Effect of movement type and rate.J Neurophysiol. 1999; 81: 3065-3077
- Medial frontal cortex: From self-generated action to reflection on one’s own performance.Trends Cogn Sci. 2010; 14: 16-21
- Neuronal activity in the primate supplementary, pre-supplementary and premotor cortex during externally and internally instructed sequential movements.Neurosci Res. 1994; 20: 149-155
- Action and the fallacy of the ‘internal’: Comment on Passingham et al.Trends Cogn Sci. 2010; 14 (author reply 193–194): 192-193
- Localization of a neural system for error detection and compensation.Psychol Sci. 1994; 5: 303-305
- The dorsal medial frontal cortex is sensitive to time on task, not response conflict or error likelihood.NeuroImage. 2011; 57: 303-311
- Checking behavior in rhesus monkeys is related to anxiety and frontal activity.Sci Rep. 2017; 745267
- How confident do you feel?.Neuron. 2014; 83: 751-753
- A non-invasive head-holding device for chronic neural recordings in awake behaving monkeys.J Neurosci Methods. 2015; 240: 154-160
- Using neuronal latency to determine sensory-motor processing pathways in reaction time tasks.J Neurophysiol. 2005; 93: 2974-2986
- Comparison of two populations of curves with an application in neuronal data analysis.Stat Med. 2011; 30: 1441-1454
- A mathematical framework for statistical decision confidence.Neural Comput. 2016; 28: 1840-1858
- When to act, or not to act: That’s the SMA’s question.Curr Opin Behav Sci. 2016; 8: 14-21
- Response inhibition and response selection: Two sides of the same coin.J Cogn Neurosci. 2008; 20: 751-761
- Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey.J Comp Neurol. 1993; 338: 114-140
- Thalamocortical and intracortical connections of monkey cingulate motor areas.J Comp Neurol. 2003; 462: 121-138
- Imaging the premotor areas.Curr Opin Neurobiol. 2001; 11: 663-672
- The origin of corticospinal projections from the premotor areas in the frontal lobe.J Neurosci. 1991; 11: 667-689
- Cortical control of reaching movements.Curr Opin Neurobiol. 1997; 7: 849-859
- Neurons in the rostral cingulate motor area monitor multiple phases of visuomotor behavior with modest parametric selectivity.J Neurophysiol. 2005; 94: 640-656
- Human presupplementary motor area is active before voluntary movement: Subdural recording of bereitschaftspotential from medial frontal cortex.Exp Brain Res. 2000; 131: 165-177
- Medial prefrontal cell activity signaling prediction errors of action values.Nat Neurosci. 2007; 10: 647-656
- Single medial prefrontal neurons cope with error.PLoS One. 2009; 4e6240
- Electrophysiological correlates of a versatile executive control system in the monkey anterior cingulate cortex.Cereb Cortex. 2016; 26: 1684-1697
- Spatial distribution of cingulate cells projecting to the primary, supplementary, and pre-supplementary motor areas: A retrograde multiple labeling study in the macaque monkey.Neurosci Res. 2001; 39: 39-49
- Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning.Brain Cogn. 2004; 56: 129-140
- Specific frontal neural dynamics contribute to decisions to check.Nat Commun. 2016; 711990
- Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey.J Comp Neurol. 1999; 410: 343-367
- Cortex and Mind: Unifying Cognition.Oxford University Press, Oxford2002
- Neural evidence accumulation persists after choice to inform metacognitive judgments.eLife. 2015; 4: 3478
- Switching from automatic to controlled action by monkey medial frontal cortex.Nat Neurosci. 2007; 10: 240-248
- Functional neuroanatomy of the primate isocortical motor system.Anat Embryol (Berl). 2000; 202: 443-474
- The organization of the cortical motor system: New concepts.Electroencephalogr Clin Neurophysiol. 1998; 106: 283-296
- Reciprocal interactions of the SMA and cingulate cortex sustain premovement activity for voluntary actions.J Neurosci. 2014; 34: 16397-16407
- Modeling psychiatric disorders for developing effective treatments.Nat Med. 2015; 21: 979-988
- Functions of frontostriatal systems in cognition: Comparative neuropsychopharmacological studies in rats, monkeys and humans.Biol Psychol. 2006; 73: 19-38
- Evolution of the neocortex: A perspective from developmental biology.Nat Rev Neurosci. 2009; 10: 724-735
- Cingulate Neurobiology and Disease.Oxford University Press, Oxford2009
Article Info
Publication History
Published online: May 27, 2022
Accepted:
May 18,
2022
Received in revised form:
April 15,
2022
Received:
June 12,
2021
Publication stage
In Press Journal Pre-ProofIdentification
Copyright
© 2022 Society of Biological Psychiatry.
