J Physiol 0.
0 (2021) pp 1–2
C R O S S TA L K
Rebuttal from Michael Dimitriou
Michael Dimitriou
Physiology Section, Department of
Integrative Medical Biology, University
of Umeå, Umeå, Sweden
Email: mdimitriou@umu.se
Edited by: Francisco Sepúlveda & Vaughan
Macefield
Linked articles: This article is part of a
CrossTalk debate. Click the links to read
the other articles in this debate: https://
doi.org/10.1113/JP281337, https://doi.org/
10.1113/JP281338, https://doi.org/10.1113/
JP281594.
TheJournalofPhysiology
In his concluding remarks (Burke, 2021),
the honourable opponent states that ‘the
field has been hampered by the belief that
everything functions as in the cat and
that we would see this if only we could
study humans behaving like cats.’ Whether
or not the field has been hampered by
such a belief, the present author does not
believe that fusimotor control in humans
and cats must necessarily be the same.
Indeed, it is reasonable to expect functional
particularities in fusimotor control, not only
across species but across lower and upper
human limbs as well. That said, strong
evidence of independent fusimotor control
in one mammalian species does motivate
the search for fusimotor independence in
another.
Despite having to support that humans
have little to gain from independent
fusimotor control, the opponent
nevertheless concludes that ‘Fusimotor
motorneurones can be activated pre-
ferentially, even selectively in humans,’ and
‘It is conceivable that selective changes in
fusimotor drive play an important role in
kinaesthesia and in providing the feedback
necessary for performing and updating a
movement’ (Burke, 2021). As described
in the CrossTalk proposal (Dimitriou,
2021), one of our studies (Dimitriou,
2016) has already demonstrated a quite
dramatic spindle ‘linearization’ effect when
there is a need to (re-) adapt internal
models following the sudden removal of
© 2021 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution
and reproduction in any medium, provided the original work is properly cited.
a visual perturbation (‘washout’ stage).
The selective extraction of information is a
known component in motor learning, but
only the selective processing of information
and the effective placement of sensors
(i.e. anticipating where to look) have been
previously emphasized; see e.g. Wolpert
et al. (2011) for a review. To our knowledge,
no other study has recorded from spindle
afferents during washout (such details are
potentially very important for appropriate
knowledge synthesis). The opponent
also comments that ‘It is conceivable
that stimulation of cutaneous receptors
during natural movements may have been
responsible for some of the positive findings
during movement.’ In our 2016 study, there
is no reason to believe that cutaneous
stimulation of the freely moving hand
was different overall as a function of task
stage.
The opponent also states that ‘Burke et al.
(1980) found no evidence for a selective
effect on fusimotor neurones when sub-
jects were given warning cues so that
they could anticipate a signal to contract,
but Papaioannou & Dimitriou (2021)
report that, in a reaching paradigm, pre-
paration for movement can involve tuning
of spindle receptors.’ To our knowledge,
our study (Papaioannou & Dimitriou,
2021) is the first to record from spindle
afferents in a context involving both a
dedicated preparatory delay and actual
voluntary movements. These centre-out
movements were performed at the level
of the upper limb, further paralleling
previous relevant work with non-human
primates. In contrast, the study of Burke
et al. (1980) involved preparing and making
an anticipatory contraction that would
prevent an imposed movement of the
foot about the ankle. Again, such details
are potentially important for appropriate
knowledge synthesis. In addition to a
possible difference in the fusimotor control
of the hand and the foot, the intention to
perform a goal-directed movement may
be necessary for invoking preparatory
proprioceptive control. The opponent
also concludes that there is little evidence
that independent fusimotor control is a
mechanism for changing the gain of stretch
reflexes. Our 2021 paper includes two
1
well-controlled follow-up experiments
demonstrating a congruent preparatory
modulation of stretch reflex gains across
different shoulder and upper arm muscles.
Our findings are compatible with the
independent, top-down and goal-directed
control of primary spindle receptors during
movement preparation (see the Discussion
section of the aforementioned paper for
more details). Additional studies shall soon
follow.
Call for comments
Readers are invited to give their views
on this and the accompanying Cross-
Talk articles in this issue by submitting
a brief (250 word) comment. Comments
may be submitted up to 6 weeks after
publication of the article, at which point
the discussion will close and the Cross-
Talk authors will be invited to submit a
‘Last Word’. Please email your comment,
including a title and a declaration of inter-
est, to jphysiol@physoc.org. Comments will
be moderated and accepted comments will
be published online only as ‘supporting
information’ to the original debate articles
once discussion has closed.
References
Burke D (2021). CrossTalk opposing view:
There is little to gain from the independent
control of human muscle spindles. J Physiol,
https://doi.org/10.1113/JP281337.
Burke D, McKeon B, Skuse NF & Westerman
RA (1980). Anticipation and fusimotor
activity in preparation for a voluntary
contraction. J Physiol 306, 337–348.
Dimitriou M (2016). Enhanced muscle afferent
signals during motor learning in humans.
Curr Biol 26, 1062–1068.
Dimitriou M (2021). Crosstalk proposal:
There is much to gain from the independent
control of human muscle spindles. J Physiol,
https://doi.org/10.1113/JP281338.
Papaioannou S & Dimitriou M (2021).
Goal-dependent tuning of muscle spindle
receptors during movement preparation. Sci
Adv 7, eabe0401.
Wolpert DM, Diedrichsen J & Flanagan JR
(2011). Principles of sensorimotor learning.
Nat Rev Neurosci 12, 739–751.
DOI: 10.1113/JP281595
2 CrossTalk J Physiol 0.0

Additional information Funding Keywords

Competing interests This work was supported by grants awarded to fusimotor control, human, muscle spindle,
M.D. by the Medical Faculty of Umeå University proprioception, sensorimotor
No competing interests declared.
(strategic grant 2.1.6-1119-19) and the Swedish
Research Council (project 2020–02140). The
Author contributions views expressed in this article are the author’s
own.
Sole author.

© 2021 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society