This study tests for a function of the somatosensory
cortex, that, in addition to its role in processing
somatic afferent information, somatosensory cortex
contributes both to motor learning and the
stabilization of motor memory. Continuous theta-burst
magnetic stimulation (cTBS) was applied, before
force-field training to disrupt activity in either the
primary somatosensory cortex, primary motor cortex, or
a control zone over the occipital lobe. Tests for
retention and relearning were conducted after a 24 h
delay. Analysis of movement kinematic measures and
force-channel trials found that cTBS to somatosensory
cortex disrupted both learning and subsequent
retention, whereas cTBS to motor cortex had little
effect on learning but possibly impaired retention.
Basic movement variables are unaffected by cTBS
suggesting that the stimulation does not interfere
with movement but instead disrupts changes in the
cortex that are necessary for learning. In all
experimental conditions, relearning in an abruptly
introduced force field, which followed retention
testing, showed extensive savings, which is consistent
with previous work suggesting that more cognitive
aspects of learning and retention are not dependent on
either of the cortical zones under test. Taken
together, the findings are consistent with the idea
that motor learning is dependent on learning-related
activity in the somatosensory cortex. NEW &
NOTEWORTHY This study uses noninvasive transcranial
magnetic stimulation to test the contribution of
somatosensory and motor cortex to human motor learning
and retention. Continuous theta-burst stimulation is
applied before learning; participants return 24 h
later to assess retention. Disruption of the
somatosensory cortex is found to impair both learning
and retention, whereas disruption of the motor cortex
has no effect on learning. The findings are consistent
with the idea that motor learning is dependent upon
learning-related plasticity in somatosensory cortex.
Kumar N, Sidarta A, Smith C, Ostry DJ, (2022)
Ventrolateral prefrontal cortex contributes to human
motor learning. eNeuro
Abstract
PDF
This study
assesses the involvement in human motor learning,
of the ventrolateral prefrontal cortex (BA 9/46v),
a somatic region in the middle frontal gyrus. The
potential involvement of this cortical area in
motor learning is suggested by studies in nonhuman
primates which have found anatomic connections
between this area and sensorimotor regions in
frontal and parietal cortex, and also with basal
ganglia output zones. It is likewise sug- gested
by electrophysiological studies which have shown
that activity in this region is implicated in
somatic sensory memory and is also influenced by
reward. We directly tested the hypothesis that
area 9/46v is in- volved in reinforcement-based
motor learning in humans. Participants performed
reaching movements to a hidden target and received
positive feedback when successful. Before the
learning task, we applied continu- ous theta burst
stimulation (cTBS) to disrupt activity in 9/46v in
the left or right hemisphere. A control group
received sham cTBS. The data showed that cTBS to
left 9/46v almost entirely eliminated motor
learning, whereas learning was not different from
sham stimulation when cTBS was applied to the same
zone in the right hemisphere. Additional analyses
showed that the basic reward-history-dependent
pattern of movements was preserved but more
variable following left hemisphere stimulation,
which suggests an overall deficit in so- matic
memory for target location or target directed
movement rather than reward processing per se. The
re- sults indicate that area 9/46v is part of the
human motor learning circuit.
Kumar N, van Vugt FT,
Ostry DJ (2021) Recognition memory for human motor
learning. Curr Biol 31:1678-1686.
Abstract
PDF
Motor skill retention is
typically measured by asking participants to
reproduce previously learned movements from
memory. The analog of this retention test (recall
memory) in human verbal memory is known to
under-estimate how much learning is actually
retained. Here we asked whether information about
previously learned movements, which can no longer
be reproduced, is also retained. Following
visuomotor adaptation,we used tests of recall that
involved reproduction of previously learned
movements and tests of recognition in which
participants were asked whether a candidate limb
displacement, produced by a robot arm held by the
subject, corresponded to a movement direction that
was experienced during active training. The main
finding was that 24 h after training, estimates of
recognition memory were about twice as accurate as
those of recall memory. Thus, there is information
about previously learned movements that is not
retrieved using recall testing but can be accessed
in tests of recognition. We conducted additional
tests to assess whether,24 h after learning,
recall for previously learned movements could be
improved by presenting passive movements as
retrieval cues. These tests were conducted
immediately prior to recall testing and involved
the passive playback of a small number of
movements, which were spread across the workspace
and included both adapted and baseline movements,
without being marked as such. This technique
restored recall memory for movements to levels
close to those of recognition memory performance.
Thus, somatic information may enable retrieval of
otherwise inaccessible motor memories.
Kumar N,
Manning TF, Ostry DJ (2019) Somatosensory cortex
participates in the consolidation of human motor
memory. PLOS Biol 17(10).
Abstract
PDF
Newly learned motor skills are
initially labile and then consolidated to permit
retention. The circuits that enable the
consolidation of motor memories remain uncertain.
Most work to date has focused on primary motor
cortex, and although there is ample evidence of
learning-related plasticity in motor cortex,
direct evidence for its involvement in memory
consolidation is limited. Learning-related
plasticity is also observed in somatosensory
cortex, and accordingly, it may also be involved
in memory consolidation. Here, by using
transcranial magnetic stimulation (TMS) to block
consolidation, we report the first direct evidence
that plasticity in somatosensory cortex
participates in the consolidation of motor memory.
Participants made movements to targets while a
robot applied forces to the hand to alter
somatosensory feedback. Immediately following
adaptation, continuous theta-burst transcranial
magnetic stimulation (cTBS) was delivered to block
retention; then, following a 24-hour delay, which
would normally permit consolidation, we assessed
whether there was an impairment. It was found that
when mechanical loads were introduced gradually to
engage implicit learning processes, suppression of
somatosensory cortex following training almost
entirely eliminated retention. In contrast, cTBS
to motor cortex following learning had little
effect on retention at all; retention following
cTBS to motor cortex was not different than
following sham TMS stimulation. We confirmed that
cTBS to somatosensory cortex interfered with
normal sensory function and that it blocked motor
memory consolidation and not the ability to
retrieve a consolidated motor memory. In
conclusion, the findings are consistent with the
hypothesis that in adaptation learning,
somatosensory cortex rather than motor cortex is
involved in the consolidation of motor memory.
Ohashi
H, Gribble PL, Ostry DJ (2019) Somatosensory
cortical excitability changes precede those in
motor cortex during human motor learning. J
Neurophysiol 122:1397-1405.
Abstract
PDF
One of the puzzles of learning to
talk or play a musical instrument is how we learn
which movement produces a particular sound: an
audiomotor map. The initial stages of map
acquisition can be studied by having participants
learn arm movements to auditory targets. The key
question is what mechanism drives this early
learning. Three learning processes from previous
literature were tested: map learning may rely on
active motor outflow, (target) error correction
and on the correspondence between sensory and
motor distances (i.e. that similar movements map
to similar sounds). Alternatively, we hypothesized
that map learning can proceed without these.
Participants made movements which were mapped to
sounds in a number of different conditions that
each precluded one of the potential learning
processes. We tested whether map learning relies
on assumptions about topological continuity by
exposing participants to a permuted map that did
not preserve distances in auditory and motor
space. Further groups were tested who passively
experienced the targets, kinematic trajectories
produced by a robot arm, and auditory feedback as
a yoked active participant (hence without active
motor outflow). Another group made movements
without receiving targets (thus without
experiencing errors). In each case we observed
substantial learning, therefore none of the three
hypothesized processes is required for learning.
Instead early map acquisition can occur with free
exploration without target error correction, is
based on sensory-to-sensory correspondences, and
possible even for discontinuous maps. The findings
are consistent with the idea that early
sensorimotor map formation can involve
instance-specific learning.
Ostry DJ, Gribble PL (2016) Sensory plasticity in
human motor learning. Trends Neurosci 39:114-123.
Abstract
PDF
There is accumulating evidence
from behavioral, neurophysiological, and
neuroimaging studies that the acquisition of motor
skills involves both perceptual and motor
learning. Perceptual learning alters movements,
motor learning, and motor networks of the brain.
Motor learning changes perceptual function and the
sensory circuits of the brain. Here, we review
studies of both human limb movement and speech
that indicate that plasticity in sensory and motor
systems is reciprocally linked. Taken together,
this points to an approach to motor learning in
which perceptual learning and sensory plasticity
have a fundamental role. Trends Sensorimotor
adaptation results in changes to sensory systems
and sensory networks in the brain. Perceptual
learning modifies sensory systems and directly
alters the motor networks of the brain. Perceptual
changes associated with sensorimotor adaptation
are durable and occur in parallel with motor
learning.
Bernardi NF, Darainy M, Ostry DJ (2015)
Somatosensory contribution to the early stages of
motor skill learning. J Neurosci 35: 14316 -14326.
Abstract PDF
The early stages of motor skill
acquisition are often marked by uncertainty about
the sensory and motor goals of the task, as is the
case in learning to speak or learning the feel of
a good tennis serve. Here we present an
experimental model of this early learning process,
in which targets are acquired by exploration and
reinforcement rather than sensory error. We use
this model to investigate the relative
contribution of motor and sensory factors to human
motor learning. Participants make active reaching
movements or matched passive movements to an
unseen target using a robot arm. We find that
learning through passive movements paired ith
reinforcement is comparable with learning
associated with active movement, both in terms of
magnitude and durability, with improvements due to
training still observable at a 1 week retest.
Motor learning is also accompanied by changes in
somatosensory perceptual acuity. No stable changes
in motor performance are observed for participants
that train, actively or passively, in the absence
of reinforcement, or for participants who are
given explicit information about target position
in the absence of somatosensory experience. These
findings indicate that the somatosensory system
dominates learning in the early stages of motor
skill acquisition.
Vahdat S, Darainy M, Ostry DJ (2014) Structure of
plasticity in human sensory and motor networks due
to perceptual learning. J Neurosci 34:2451-63.
Abstract PDF
As we begin to acquire a new motor
skill, we face the dual challenge of determining
and refining the somatosensory goals of our
movements and establishing the best motor commands
to achieve our ends. The two typically proceed in
parallel, and accordingly it is unclear how much
of skill acquisition is a reflection of changes in
sensory systems and how much reflects changes in
the brain's motor areas. Here we have
intentionally separated perceptual and motor
learning in time so that we can assess functional
changes to human sensory and motor networks as a
result of perceptual learning. Our subjects
underwent fMRI scans of the resting brain before
and after a somatosensory discrimination task. We
identified changes in functional connectivity that
were due to the effects of perceptual learning on
movement. For this purpose, we used a neural model
of the transmission of sensory signals from
perceptual decision making through to motor
action. We used this model in combination with a
partial correlation technique to parcel out those
changes in connectivity observed in motor systems
that could be attributed to activity in sensory
brain regions. We found that, after removing
effects that are linearly correlated with
somatosensory activity, perceptual learning
results in changes to frontal motor areas that are
related to the effects of this training on motor
behavior and learning. This suggests that
perceptual learning produces changes to frontal
motor areas of the brain and may thus contribute
directly to motor learning.
Darainy M, Vahdat S, Ostry DJ (2013) Perceptual
learning in sensorimotor adaptation. J Neurophysiol
110: 2152-2162.
Abstract
PDF
Motor learning often involves
situations in which the somatosensory targets of
movement are initially, poorly defined, as for
example, in learning to speak or learning the feel
of a proper tennis serve. Under these conditions,
motor skill acquisition presumably requires
perceptual as well as motor learning. That is, it
engages both the progressive shaping of sensory
targets and associated changes in motor
performance. In the present paper, we test the
idea that perceptual learning alters somatosensory
function and in so doing produces changes to motor
performance and sensorimotor adaptation. Subjects
in these experiments undergo perceptual training
in which a robotic device passively moves the arm
on one of a set of fan shaped trajectories.
Subjects are required to indicate whether the
robot moved the limb to the right or the left and
feedback is provided. Over the course of training
both the perceptual boundary and acuity are
altered. The perceptual learning is observed to
improve both the rate and extent of learning in a
subsequent sensorimotor adaptation task and the
benefits persist for at least 24 hours. The
improvement in the present studies is obtained
regardless of whether the perceptual boundary
shift serves to systematically increase or
decrease error on subsequent movements. The
beneficial effects of perceptual training are
found to be substantially dependent upon
reinforced decision-making in the sensory domain.
Passive-movement training on its own is less able
to alter subsequent learning in the motor system.
Overall, this study suggests perceptual learning
plays an integral role in motor learning.
Vahdat S, Darainy M, Milner TE, Ostry DJ
(2011) Functionally specific changes in
resting-state sensorimotor networks after motor
learning. J Neurosci 31:16907-16915.
Abstract
PDF
Motor learning changes the
activity of cortical motor and subcortical areas
of the brain, but does learning affect sensory
systems as well? We examined inhumansthe effects
of motor learning using fMRI measures of
functional connectivity under resting conditions
and found persistent changes in networks involving
both motor and somatosensory areas of the brain.
We developed a technique that allows us to
distinguish changes in functional connectivity
that can be attributed to motor learning from
those that are related to perceptual changes that
occur in conjunction with learning. Using this
technique, we identified a new network in motor
learning involving second somatosensory cortex,
ventral premotor cortex, and supplementary motor
cortex whose activation is specifically related to
perceptual changes that occur in conjunction with
motor learning. We also found changes in a network
comprising cerebellar cortex, primary motor
cortex, and dorsal premotor cortex that were
linked to the motor aspects of learning. In each
network, we observed highly reliable linear
relationships between neuroplastic changes and
behavioral measures of either motor learning or
perceptual function. Motor learning thus results
in functionally specific changes to distinct
resting-state networks in the brain.
Ostry DJ, Darainy M, Mattar AAG, Wong J, Gribble PL
(2010) Somatosensory plasticity and motor learning.
J Neurosci 30:5384-5393.
Abstract
PDF
Motor learning is dependent upon
plasticity in motor areas of the brain, but does
it occur in isolation, or does it also result in
changes to sensory systems? We examined changes to
somatosensory function that occur in conjunction
with motor learning. We found that even after
periods of training as brief as 10 min, sensed
limb position was altered and the perceptual
change persisted for 24 h. The perceptual change
was reflected in subsequent movements; limb
movements following learning deviated from the
prelearning trajectory by an amount that was not
different in magnitude and in the same direction
as the perceptual shift. Crucially, the perceptual
change was dependent upon motor learning. When the
limb was displaced passively such that subjects
experienced similar kinematics but without
learning, no sensory change was observed. The
findings indicate that motor learning affects not
only motor areas of the brain but changes sensory
function as well.