You are on page 1of 2

Opinion

Mapping Psychomotor Behavior in the Brain


VIEWPOINT

Sebastian Walther, MD Abnormal psychomotor behavior is a core feature of frontal or limbic inputs to M1 to drive alterations from
Department of psychotic and mood disorders. Disorganized and/or cata- normal motor control (ie, psychomotor disturbances).
Psychiatry and tonic behavior is 1 of 5 DSM-5-TR criterion A symptoms This interpretation assumed energetically costly long-
Behavioral Sciences,
for schizophrenia, while psychomotor retardation and/or range connectivity (eg, amygdala to M1) to be continu-
Vanderbilt University
Medical Center, agitation is 1 of 9 criterion A symptoms for a major de- ously in play during psychomotor phenomena (Figure).
Nashville, Tennessee; pressive episode and 1 of 7 criterion B symptoms for a A recent study by Gordon et al7 radically revised the
and Translational manic episode. In addition, psychomotor abnormali- standard model and redrew the M1 homunculus. Using
Research Center,
University Hospital of
ties are associated features for several other disorders, resting-state functional magnetic resonance imaging
Psychiatry and including autism spectrum and neurocognitive disor- data from 4 large cohorts with more than 8900 partici-
Psychotherapy, ders. Crucially, abnormal psychomotor behavior is as- pants and intense resting-state mapping (>3 hours) and
University of Bern,
sociated with poor clinical and functional outcomes.1 precision functional mapping in 7 participants, the au-
Bern, Switzerland.
What qualifies as abnormal psychomotor behav- thors failed to detect the textbook pattern of homoge-
Stephan Heckers, MD, ior? It refers to a person moving not enough, too much, neous connectivity with homotopic regions. Instead,
MSc or in an unusual fashion. Wernicke labeled these as they found effector regions for hand, foot, and mouth
Department of hypokinetic, hyperkinetic, and parakinetic behaviors, re- that share close connectivity to the contralateral M1 and
Psychiatry and
spectively. He proposed that their study is the royal road primary sensory cortex. Crucially, they detected, imme-
Behavioral Sciences,
Vanderbilt University to mapping the neural basis of psychiatric disorders. diately adjacent to effector regions, intereffector re-
Medical Center, Wernicke distinguished 2 stages of processing motor- gions (IERs), which have a distinct connectivity pat-
Nashville, Tennessee. related information in the brain. The first stage in- tern: increased connectivity to the SMA, cingulate motor
cluded complex volitional, affective, and cognitive as- area, insula, striatum, thalamus, and cerebellum. The 3
pects, which remain hidden from the observer, termed IERs are located between the effector regions for hand,
“psychomotor.” The second stage was the generation of foot, and mouth. Activation of these regions lacked
motor output, resulting in an observable change in be- movement specificity but was seen during movement
havior, previously termed “motor.” Broca’s description planning. The authors suspected that IERs constitute a
of motor aphasia and Hitzig’s and Fritsch’s cortical stimu- somato-cognitive action system for planning, prepar-
lation experiments in dogs gave Wernicke confidence to ing, and controlling body movements.7 The proposed or-
localize the second stage to the precentral gyrus and ganization of M1 parallels findings from monkey stud-
inferior frontal cortex. He did not localize psychomotor ies indicating nearest-neighbor principles that allow
function but speculated that there is a pathway project- efficient coding for important behavioral repertoires lo-
ing from cortical regions containing concepts cally at M1.8
(“Begriffe”) to the primary motor cortex. The IERs orchestrate movement of the entire body,
For decades, we have accepted a standard model including the integration of movement plans, urges, in-
of the motor system, in the tradition of Wernicke. The teroception, somatosensory signals, and volition.7 All
motor strip (M1) takes center stage as the final output these functions are impaired in psychomotor pathol-
region. Three subcircuits with distinct functions pro- ogy, including catatonia, psychomotor retardation, tics,
vide input to M1: (1) the basal ganglia circuit (M1-striatum- neurological soft signs, and functional neurological dis-
thalamus-M1) modulates excitation and inhibition of orders. An efficient design would place psychomotor re-
movements; (2) the cerebello-thalamo-motor circuit pro- gions close to the motor regions to integrate multiple as-
cesses sensorimotor dynamics, such as coordination, pects of complex motor behavior. Local projections cost
timing, and sequencing; and (3) cortico-motor circuits, less energy than long-range connections. These short-
including the ventromedial prefrontal cortex, anterior range connections would be developed especially dur-
cingulate cortex, supplementary motor area (SMA), M1, ing training processes and brain maturation when form-
and posterior parietal cortex, control psychomotor or- ing complex psychomotor repertoires. If IERs are the
ganization and speed.2 integrators of multiple sources of information shaping
Neuroimaging studies in depression and psychosis motor behavior, these areas would be critical for
indicated that hypokinetic motor abnormalities, such as psychomotor behaviors in psychiatric patients: ambi-
Corresponding
Author: Sebastian catatonia or psychomotor retardation, were linked to tendency and negativism, posturing and stereotypies,
Walther, MD, altered resting-state functional connectivity or cere- and stupor and mutism. Likewise, IERs should present
Translational Research bral blood flow in premotor areas and M1.3-5 Similarly, dy- altered functional connectivity in individuals with psy-
Center, University
Hospital of Psychiatry
namic resting-state connectivity in autism suggested that chomotor retardation in depression or psychosis. Fur-
and Psychotherapy, severity of repetitive motor actions was linked to less thermore, repetitive and enduring aberrant movement
University of Bern, flexible interactions between cortical (M1 and SMA) and repertoires, such as mannerisms, grimacing, or rituals,
Murtenstrasse 21,
subcortical motor networks.6 Thus, both concepts and are probably encoded in the IERs. Psychiatric neuroim-
3008 Bern,
Switzerland (sebastian. data on psychomotor behaviors indicated a role of SMA aging studies should focus specifically on the precen-
walther@unibe.ch). and M1. However, the interpretation considered pre- tral gyrus, a previously undervalued area.

jamapsychiatry.com (Reprinted) JAMA Psychiatry January 2024 Volume 81, Number 1 7

© 2023 American Medical Association. All rights reserved.


Downloaded from jamanetwork.com by Aadityarajsinh Gohil on 01/04/2024
Opinion Viewpoint

Figure. Traditional and Revised Model of Motor Strip (M1) Connectivity in Psychomotor Behaviors

Traditional model Revised model


Supplementary Primary Supplementary Primary
motor area motor cortex motor area motor cortex
Presupplementary Presupplementary
motor area motor area
Foot

Foot Sup

Hand
Hand
Med

Mouth Mouth
Mou
utth
t

Inf

Putamen Putamen
Thalamus Thalamus

Limbic Limbic
system system

Cerebellum Cerebellum

Psychomotor
Motor
Motor output

The traditional model suspected multiple unspecific inputs to the homotopically M1. Intereffectors are likely critical hubs to multiple psychomotor behaviors in
organized motor strip. The revised model includes specific intereffector regions mental illness, such as catatonia, neurological soft signs, or functional
that receive multiple inputs and orchestrate the motor effector regions within neurological disorders. Inf indicates inferior; Med, medial; Sup, superior.

Are we closer to a more sophisticated understanding of mechanistic understanding. In addition, a revised model of the
psychomotor behavior? A refined neuroanatomical model of human motor system will facilitate the development of noninva-
psychomotor behavior will focus attention on this often-ignored sive brain stimulation techniques aimed at ameliorating psycho-
domain of psychopathology. To capitalize on the novel ideas of motor symptoms. Previous studies of psychomotor abnormalities
mapping psychomotor function to the brain, we need to train cli- targeted the SMA or cerebellum,9,10 but maybe the precentral
nicians to assess psychomotor behavior in regular clinical care. gyrus is also a worthwhile target. The newly detected IERs in M1
Likewise, precise mapping of psychomotor abnormalities with might be 1 of the psychomotor pathways that Wernicke had
instrumentation (eg, with wearable devices) will support a more proposed.

ARTICLE INFORMATION 2. Mittal VA, Bernard JA, Northoff G. What can predict distinct restricted and repetitive behaviors
Published Online: November 22, 2023. different motor circuits tell us about psychosis? in children with autism. Nat Commun. 2021;12(1):
doi:10.1001/jamapsychiatry.2023.4290 Schizophr Bull. 2017;43(5):949-955. doi:10.1093/ 3537. doi:10.1038/s41467-021-23822-5
schbul/sbx087 7. Gordon EM, Chauvin RJ, Van AN, et al.
Conflict of Interest Disclosures: Dr Walther
reported receiving personal fees from Neurolite, 3. Walther S, Schäppi L, Federspiel A, et al. A somato-cognitive action network alternates with
Lundbeck, and Mepha for medical education events Resting-state hyperperfusion of the supplementary effector regions in motor cortex. Nature. 2023;617
outside the submitted work. Dr Heckers reported motor area in catatonia. Schizophr Bull. 2017;43(5): (7960):351-359. doi:10.1038/s41586-023-05964-2
receiving grants from the National Institutes of 972-981. doi:10.1093/schbul/sbw140 8. Graziano MSA. Fundamental principles of
Health outside the submitted work and was an 4. Walther S, Stegmayer K, Federspiel A, Bohlhalter cortical organization reflected in a new study. Neuron.
editor of the DSM-5-TR Schizophrenia Spectrum and S, Wiest R, Viher PV. Aberrant hyperconnectivity in 2023;111(10):1524-1525. doi:10.1016/j.neuron.2023.
Other Psychotic Disorders section. the motor system at rest is linked to motor 04.024
Additional Contributions: Michael Linkinhoker, abnormalities in schizophrenia spectrum disorders. 9. Gupta T, Dean DJ, Kelley NJ, Bernard JA,
MA (Link Studio), created the figure and was Schizophr Bull. 2017;43(5):982-992. doi:10.1093/ Ristanovic I, Mittal VA. Cerebellar transcranial direct
compensated. schbul/sbx091 current stimulation improves procedural learning in
5. Cantisani A, Stegmayer K, Bracht T, et al. Distinct nonclinical psychosis. Schizophr Bull. 2018;44(6):
REFERENCES resting-state perfusion patterns underlie 1373-1380. doi:10.1093/schbul/sbx179
1. Pieters LE, Nadesalingam N, Walther S, van psychomotor retardation in unipolar vs bipolar 10. Walther S, Alexaki D, Schoretsanitis G, et al.
Harten PN. A systematic review of the prognostic depression. Acta Psychiatr Scand. 2016;134(4):329- Inhibitory repetitive transcranial magnetic
value of motor abnormalities on clinical outcome in 338. doi:10.1111/acps.12625 stimulation to treat psychomotor slowing.
psychosis. Neurosci Biobehav Rev. 2022;132:691-705. 6. Supekar K, Ryali S, Mistry P, Menon V. Aberrant Schizophr Bull Open. 2020;1(1):sgaa020. doi:10.
doi:10.1016/j.neubiorev.2021.11.027 dynamics of cognitive control and motor circuits 1093/schizbullopen/sgaa020

8 JAMA Psychiatry January 2024 Volume 81, Number 1 (Reprinted) jamapsychiatry.com

© 2023 American Medical Association. All rights reserved.


Downloaded from jamanetwork.com by Aadityarajsinh Gohil on 01/04/2024

You might also like