What can crossmodal aftereffects reveal about neural representation and dynamics?
Identifieur interne : 000C27 ( Pmc/Curation ); précédent : 000C26; suivant : 000C28What can crossmodal aftereffects reveal about neural representation and dynamics?
Auteurs : Talia Konkle ; Christopher I. MooreSource :
- Communicative & Integrative Biology [ 1942-0889 ] ; 2009.
Abstract
The brain continuously adapts to incoming sensory stimuli, which can lead to perceptual
illusions in the form of aftereffects. Recently we demonstrated that motion aftereffects
transfer between vision and touch.
Url:
DOI: 10.4161/cib.2.6.9344
PubMed: 22811763
PubMed Central: 3398893
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">What can crossmodal aftereffects reveal about neural representation and
dynamics?</title><author><name sortKey="Konkle, Talia" sort="Konkle, Talia" uniqKey="Konkle T" first="Talia" last="Konkle">Talia Konkle</name><affiliation><nlm:aff id="A1">McGovern Institute for Brain Research; Massachusetts Institute of Technology</nlm:aff></affiliation><affiliation><nlm:aff id="A2">Department of Brain & Cognitive Sciences; Massachusetts Institute of Technology</nlm:aff></affiliation></author><author><name sortKey="Moore, Christopher I" sort="Moore, Christopher I" uniqKey="Moore C" first="Christopher I." last="Moore">Christopher I. Moore</name><affiliation><nlm:aff id="A1">McGovern Institute for Brain Research; Massachusetts Institute of Technology</nlm:aff></affiliation><affiliation><nlm:aff id="A2">Department of Brain & Cognitive Sciences; Massachusetts Institute of Technology</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22811763</idno><idno type="pmc">3398893</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3398893</idno><idno type="RBID">PMC:3398893</idno><idno type="doi">10.4161/cib.2.6.9344</idno><date when="2009">2009</date><idno type="wicri:Area/Pmc/Corpus">000C27</idno><idno type="wicri:Area/Pmc/Curation">000C27</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">What can crossmodal aftereffects reveal about neural representation and
dynamics?</title><author><name sortKey="Konkle, Talia" sort="Konkle, Talia" uniqKey="Konkle T" first="Talia" last="Konkle">Talia Konkle</name><affiliation><nlm:aff id="A1">McGovern Institute for Brain Research; Massachusetts Institute of Technology</nlm:aff></affiliation><affiliation><nlm:aff id="A2">Department of Brain & Cognitive Sciences; Massachusetts Institute of Technology</nlm:aff></affiliation></author><author><name sortKey="Moore, Christopher I" sort="Moore, Christopher I" uniqKey="Moore C" first="Christopher I." last="Moore">Christopher I. Moore</name><affiliation><nlm:aff id="A1">McGovern Institute for Brain Research; Massachusetts Institute of Technology</nlm:aff></affiliation><affiliation><nlm:aff id="A2">Department of Brain & Cognitive Sciences; Massachusetts Institute of Technology</nlm:aff></affiliation></author></analytic><series><title level="j">Communicative & Integrative Biology</title><idno type="eISSN">1942-0889</idno><imprint><date when="2009">2009</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The brain continuously adapts to incoming sensory stimuli, which can lead to perceptual
illusions in the form of aftereffects. Recently we demonstrated that motion aftereffects
transfer between vision and touch.<xref ref-type="bibr" rid="R1"><sup>1</sup></xref> Here,
the adapted brain state induced by one modality has consequences for processes in another
modality, implying that somewhere in the processing stream, visual and tactile motion have
shared underlying neural representations. We propose the adaptive processing
hypothesis—any area that processes a stimulus adapts to the features of the stimulus it
represents, and this adaptation has consequences for perception. This view argues that
there is no single locus of an aftereffect. Rather, aftereffects emerge when the test
stimulus used to probe the effect of adaptation requires processing of a given type. The
illusion will reflect the properties of the brain area(s) that support that specific level
of representation. We further suggest that many cortical areas are more process-dependent
than modality-dependent, with crossmodal interactions reflecting shared processing demands
in even ‘early’ sensory cortices.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Konkle, T" uniqKey="Konkle T">T Konkle</name></author><author><name sortKey="Wang, Q" uniqKey="Wang Q">Q Wang</name></author><author><name sortKey="Hayward, V" uniqKey="Hayward V">V Hayward</name></author><author><name sortKey="Moore, Ci" uniqKey="Moore C">CI Moore</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wolgemuth, A" uniqKey="Wolgemuth A">A Wolgemuth</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mather, G" uniqKey="Mather G">G Mather</name></author><author><name sortKey="Pavan, A" uniqKey="Pavan A">A Pavan</name></author><author><name sortKey="Campana, G" uniqKey="Campana G">G Campana</name></author><author><name sortKey="Casco, C" uniqKey="Casco C">C Casco</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Grantham, Dw" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Commun Integr Biol</journal-id><journal-id journal-id-type="iso-abbrev">Commun Integr Biol</journal-id><journal-id journal-id-type="publisher-id">CIB</journal-id><journal-title-group><journal-title>Communicative & Integrative Biology</journal-title></journal-title-group><issn pub-type="epub">1942-0889</issn><publisher><publisher-name>Landes Bioscience</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22811763</article-id><article-id pub-id-type="pmc">3398893</article-id><article-id pub-id-type="publisher-id">2009CIB0035</article-id><article-id pub-id-type="pii">9344</article-id><article-id pub-id-type="doi">10.4161/cib.2.6.9344</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article Addendum</subject></subj-group></article-categories><title-group><article-title>What can crossmodal aftereffects reveal about neural representation and
dynamics?</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Konkle</surname><given-names>Talia</given-names></name><xref ref-type="aff" rid="A1"><sup>1</sup></xref><xref ref-type="aff" rid="A2"><sup>2</sup></xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><contrib contrib-type="author"><name><surname>Moore</surname><given-names>Christopher I.</given-names></name><xref ref-type="aff" rid="A1"><sup>1</sup></xref><xref ref-type="aff" rid="A2"><sup>2</sup></xref></contrib><aff id="A1"><label>1</label>McGovern Institute for Brain Research; Massachusetts Institute of Technology</aff><aff id="A2"><label>2</label>Department of Brain & Cognitive Sciences; Massachusetts Institute of Technology</aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>Correspondence to: Talia Konkle, Email: <email xlink:href="cim@mit.edu">cim@mit.edu</email></corresp></author-notes><pub-date pub-type="ppub"><season>Nov-Dec</season><year>2009</year></pub-date><pub-date pub-type="pmc-release"><day>1</day><month>11</month><year>2009</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>2</volume><issue>6</issue><fpage>479</fpage><lpage>481</lpage><permissions><copyright-statement>Copyright © 2009 Landes Bioscience</copyright-statement><copyright-year>2009</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/"><license-p>This is an open-access article licensed under a Creative Commons
Attribution-NonCommercial 3.0 Unported License. The article may be redistributed,
reproduced, and reused for non-commercial purposes, provided the original source is
properly cited.</license-p></license></permissions><abstract><p>The brain continuously adapts to incoming sensory stimuli, which can lead to perceptual
illusions in the form of aftereffects. Recently we demonstrated that motion aftereffects
transfer between vision and touch.<xref ref-type="bibr" rid="R1"><sup>1</sup></xref> Here,
the adapted brain state induced by one modality has consequences for processes in another
modality, implying that somewhere in the processing stream, visual and tactile motion have
shared underlying neural representations. We propose the adaptive processing
hypothesis—any area that processes a stimulus adapts to the features of the stimulus it
represents, and this adaptation has consequences for perception. This view argues that
there is no single locus of an aftereffect. Rather, aftereffects emerge when the test
stimulus used to probe the effect of adaptation requires processing of a given type. The
illusion will reflect the properties of the brain area(s) that support that specific level
of representation. We further suggest that many cortical areas are more process-dependent
than modality-dependent, with crossmodal interactions reflecting shared processing demands
in even ‘early’ sensory cortices.</p></abstract><kwd-group kwd-group-type="author"><title>Keywords: </title><kwd>Adaptation</kwd><kwd>brain state</kwd><kwd>multisensory</kwd><kwd>motion</kwd><kwd>visual</kwd><kwd>tactile</kwd><kwd>aftereffect</kwd></kwd-group></article-meta></front><body><sec><title>Introduction</title><p>Aftereffects are a powerful behavioral paradigm used to infer how information is
represented in the brain and how neural populations and circuits change over time – neural
dynamics. In the case of motion aftereffect paradigms, for example, an observer stares at
visual motion such as a drifting grating (the adapting stimulus) for a period of seconds.
When this visual stimulus is suddenly changed to a static visual grating (the test
stimulus), the observer sees this stationary stimulus as if it were moving opposite the
direction of the original motion for a short period of time.<xref ref-type="bibr" rid="R2"><sup>2</sup></xref><sup>,</sup><xref ref-type="bibr" rid="R3"><sup>3</sup></xref> From
this simple behavioral paradigm, we gain critical insights into both underlying neural
representation and neural dynamics. First, visual motion perception relies on competing
representations in opponent directions. Second, extended processing of a stimulus leads to
changes in the brain, which we refer to as the adapted brain state. Where in the brain are
circuits changing during adaptation? In other words, what is the site of these neural
dynamics?</p><p>One intuitive answer is that visual motion aftereffects arise from local dynamics in visual
cortex. Motion aftereffects also exist in the auditory<xref ref-type="bibr" rid="R4"><sup>4</sup></xref> and tactile domains,<xref ref-type="bibr" rid="R5"><sup>5</sup></xref> suggesting that such neural dynamics are a general property of
cortico-cortical or thalamo-cortical circuits.<xref ref-type="bibr" rid="R6"><sup>6</sup></xref> However, we recently demonstrated that adaptation to tactile motion
can lead to visual motion aftereffects, and visa versa.<xref ref-type="bibr" rid="R1"><sup>1</sup></xref> Further, visual motion adaptation leads to auditory motion
aftereffects.<xref ref-type="bibr" rid="R7"><sup>7</sup></xref><sup>,</sup><xref ref-type="bibr" rid="R8"><sup>8</sup></xref> As such, these crossmodal aftereffects
challenge the simple explanation that motion aftereffects arise from unisensory cortex
alone. What properties about adaptation and representation are needed to explain how
crossmodal aftereffects occur?</p></sec><sec><title>Adaptive Processing Hypothesis</title><p>Aftereffects reveal that extended processing of incoming sensory information changes the
brain, and there are measurable consequences of this change in subsequent perception. What
is the site of these neural dynamics? A naïve view is that dynamics are expressed only in a
final integration stage, for example a single ‘higher’ order cortical area, where modulatory
flexibility is inherent to its function. In the classic view, the explicit computational
goal of this area is ‘bimodal’ integration. Cross-modal aftereffects would emerge, then, as
the product of dynamics at this convergent center.</p><p>In contrast, we propose that any area or circuit that processes a stimulus is changed by
that stimulus and that these dynamics are a functional property of areas throughout the
system—the adaptive processing hypothesis. For example, motion-responsive neurons are found
in many places short of the “motion processing area” MT, including V1, V2, and V3, and are
also found in parietal areas. Thus, motion aftereffects likely originate not from adaptation
in one area or circuit but from many stages of processing both in early sensory areas and in
higher level areas.<xref ref-type="bibr" rid="R3"><sup>3</sup></xref></p><p>A corollary of the adaptive processing hypothesis is that at each level of processing,
different aspects of the incoming stimulus are adapting, reflecting the underlying
dimensions represented by those neural populations. For example, V1 responses reflect
orientation, scale, and motion properties at a specific location, with increasing receptive
field size and tuning properties in V2, V3, and MT. This view implies that different
aftereffects might be observed across retinotopic locations based on the relative
contribution of early and later areas in processing the subsequent test stimulus.</p><p>Thus, in adaptation paradigms, the subsequent test stimulus can be thought of as a probe of
the adapted state. For example, following 10 sec of visual motion adaptation, presenting a
static grating leads to retinotopic aftereffects of short duration with low illusory
velocity. Following the same adaptation, presenting a dynamic grating instead leads to
aftereffects in more spatial locations, which have faster velocity and longer duration.<xref ref-type="bibr" rid="R9"><sup>9</sup></xref> Importantly, the same adapted brain state can
give rise to several different perceptual aftereffects. Similarly, following adaptation to a
face, observers have stronger aftereffects when tested on upright vs. inverted faces, but
also show aftereffects when tested with simple T-shaped stimuli.<xref ref-type="bibr" rid="R10"><sup>10</sup></xref><sup>,</sup><xref ref-type="bibr" rid="R11"><sup>11</sup></xref> The critical insight is that the adapted brain state will have
consequences on a subsequently presented test stimulus to the extent that that test stimulus
depends on processing in those adapted areas. This framework helps explain the well known
fact that aftereffects depend on the relationship between the adapting and test
stimuli.<xref ref-type="bibr" rid="R3"><sup>3</sup></xref></p><p>In the case of crossmodal aftereffects, these paradigms simply use one modality to probe
the adapted state induced by extended processing in another modality. For example, we
recently demonstrated that visual and tactile motion adaptation lead to aftereffects in the
other modality.<xref ref-type="bibr" rid="R1"><sup>1</sup></xref> Based on the framework
outlined above, processing tactile motion depends on circuits that were previously adapted
by visual motion processing. Similarly, the processing of visual motion depends on circuits
adapted by tactile motion. Crossmodal motion aftereffects reveal that visual and tactile
motion perception rely on partially shared neural substrates.</p></sec><sec><title>Process-Selective Cortical Circuits</title><p>One reason why there might be a site of shared processing between visual and tactile motion
comes from an argument for efficient processing. If there is a neural circuit that is
specialized to extract motion trajectories from spatio-temporal patterns of spiking input,
it might be efficient to route information that requires that processing through that
circuit. Indeed, visual motion and tactile motion appear to processed in overlapping (or at
least adjacent) areas.<xref ref-type="bibr" rid="R12"><sup>12</sup></xref><sup>,</sup><xref ref-type="bibr" rid="R13"><sup>13</sup></xref></p><p>However, this logic does not extend to auditory motion, which does not activate area
MT<xref ref-type="bibr" rid="R14"><sup>14</sup></xref> (reviewed in ref. <xref ref-type="bibr" rid="R15">15</xref>). One possible account for this discrepancy is that
visual motion and tactile motion share a similar input pattern, where a grid of sensors in
the retina or skin receives spatial information over time. Interestingly, auditory motion
information does not arrive by a grid of spatial sensors but by interaural temporal
differences, suggesting these stimuli access other brain areas organized to more efficiently
perform a different computation.</p><p>Several other examples of utilizing specialized processing circuits across modalities
exists. For example, TMS studies have shown that fine spatial orientation judgments utilize
V1 for visual as well as tactile stimuli.<xref ref-type="bibr" rid="R16"><sup>16</sup></xref> Further, fMRI evidence has shown that fine scale orientation
judgments in vision and tactile modalities both activate early visual cortex,<xref ref-type="bibr" rid="R17"><sup>17</sup></xref> visual and haptic shape activate lateral
occipital areas,<xref ref-type="bibr" rid="R18"><sup>18</sup></xref> and even haptic
exploration of faces is suggested to activate the visual face-selective FFA.<xref ref-type="bibr" rid="R19"><sup>19</sup></xref> If these areas are fundamentally
contributing to the perception of orientation, shape, and faces in both modalities, then we
would predict crossmodal aftereffects will be found. More generally, these data support
process-selective cortical circuits, rather than stimulus-selective cortical circuits.
Indeed, emerging evidence that the neocortex is more multisensory than previously
believed,<xref ref-type="bibr" rid="R20"><sup>20</sup></xref><sup>,</sup><xref ref-type="bibr" rid="R21"><sup>21</sup></xref> also suggests that defining areas by
sensory modality might not accurately describe the underlying representation.</p></sec><sec sec-type="conclusions"><title>Conclusions</title><p>Aftereffects reveal that any incoming sensory information leads to changes in neural
dynamics. Typically when we sense the world, we sample the continuous stream of input with
rapid exploratory patterns. Eyes saccade 3 times per second, and maintaining steady fixation
eventually causes the world to turn flat gray. Similarly, skin sweeps over surfaces, and
without changing stimulation we cease to notice contact, e.g., with clothing. While active
sensing rapidly samples different aspects of the physical world, adaptation paradigms force
extended processing of a single aspect of the physical world (for adaptation with brief
durations see ref. <xref ref-type="bibr" rid="R22">22</xref>). In a sense, this extended
processing during adaptation may accentuate the neural mechanisms and perceptual
consequences that are continually operating on at a more rapid timescale.</p><p>Crossmodal aftereffects provide several insights about these adaptive mechanisms.
Specifically, we suggest that adaptation is happening at all neural sites that are involved
in processing the stimulus, e.g., by renormalizing competing representations to reflect the
incoming sensory information. The test stimulus can be thought of as a probe of this adapted
state – the extent of shared substrates in processing determines what aftereffects
properties will be observed. Areas may be more process-dependent, rather than
stimulus-dependent, with crossmodal interactions following automatically in cases with
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