Current Biology

Dispatches

could be a necessary adjustment to the receptors on foveal ganglion cells) agrees the role of photoreceptor dimensions. J. Opt.
Soc. Am. A 2, 393–398.
presence of a long axon. This axon will filter with their physiology but conflicts with
rapidly varying signals, a biophysical earlier studies using electron microscopy 5. Solomon, S.G., Martin, P.R., White, A.J.,
consequence of the membrane [8–10]. Because their technique strains the Ruttiger, L., and Lee, B.B. (2002). Modulation
sensitivity of ganglion cells in peripheral retina
capacitance [7]. In that case the slower limits of light microscopy, more information of macaque. Vision Res. 42, 2893–2898.
responses in the fovea will tend to preserve will be needed to get to the bottom of this.
the size of the final output that gets to the But Sinha et al. make the important general 6. Walilko, T.J., Viano, D.C., and Bir, C.A. (2005).
Biomechanics of the head for Olympic boxer
bipolar cell: the long axon will act like a low- point that the booming connectomics punches to the face. Br. J. Sports Med. 39,
pass filter, so that slow signals are industry [11,12] is at present stuck with the 710–719.
transmitted better than fast ones. assumption that structurally similar 7. Hsu, A., Tsukamoto, Y., Smith, R.G., and
Remember that the long axon exists for synapses all have the same weight — Sterling, P. (1998). Functional architecture of
purely optical reasons, to keep the inner something unlikely to be correct. We need primate cone and rod axons. Vision Res. 38,
2539–2549.
retinal circuitry from scattering light and more test cases, situations in which
allow close packing of the cones’ light- electron microscope images of specific 8. Kolb, H., and Dekorver, L. (1991). Midget
sensitive outer segments. Thus, the synapses can be linked to their chemical ganglion cells of the parafovea of the human
retina: a study by electron microscopy and
evolutionary trade-off would sacrifice neuroanatomy and their behavior in serial section reconstructions. J. Comp.
sensitivity to rapid signals as an indirect transmitting information. Neurol. 303, 617–636.
cost of maximal spatial resolution. In the 9. Calkins, D.J., and Sterling, P. (1996). Absence
first interpretation, slow integration is REFERENCES of spectrally specific lateral inputs to midget
intrinsically a good thing. In the second, the ganglion cells in primate retina. Nature 381,
1. Sinha, R., Hoon, M., Baudin, J., Okawa, H., 613–615.
slow response is a necessary evil, where
Wong, R.O.L., and Rieke, F. (2017). Cellular
speed is sacrificed in order to allow and circuit mechanisms shaping the 10. Calkins, D.J., and Sterling, P. (2007).
something (acuity) more important. And of perceptual properties of the primate fovea. Microcircuitry for two types of achromatic
Cell 168, 413–426. ganglion cell in primate fovea. J. Neurosci. 27,
course, both things could be true. 2646–2653.
A separate but important technical point 2. Masland, R.H. (2012). The neuronal
organization of the retina. Neuron 76, 266–280. 11. Lichtman, J.W., and Denk, W. (2011). The big
is made by Sinha et al., who used high and the small: challenges of imaging the
resolution fluorescence microscopy to 3. Polyak, S.L. (1948). The Retina (University of brain’s circuits. Science 334, 618–624.
compare the inhibitory input to ganglion Chicago Press: Illinois).
12. Seung, S. (2012). Connectome: How the
cells in the fovea with those in the 4. Tyler, C.W. (1985). Analysis of visual Brain’s Wiring Makes Us Who We Are (New
periphery. Their result (few inhibitory modulation sensitivity. II. Peripheral retina and York: Houghton Mifflin).

Multisensory Development: Calibrating a Coherent

A new study reveals the effects of visual deprivation in early life on the development of multisensory
simultaneity perception. To understand the developmental processes underlying this we need to consider
the multisensory milieu of the newborn infant.

The newborn human arrives into a in almost uniformly varying neural codes. If together. A new study [1] sheds important
startlingly complex sensory world in which infants are to develop an ability to perceive light on how this happens.
it is invaded by information from touch, a spatiotemporally coherent and
taste, smell, proprioception, vestibular meaningful environment from amongst Developing Solutions to the
input, audition, and vision, all of which this multisensory me lange, they need to Crossmodal Binding Problem
provide cues about features of objects learn to solve the ‘‘crossmodal binding Whilst the advantages which multiple
and events which arrive in the central problem’’, i.e. they need to figure out how senses bestow to perception are well
nervous system at different latencies, and and when stimuli across the senses go acknowledged (e.g., [2]), the challenges

Current Biology 27, R294–R317, April 24, 2017 ª 2017 Elsevier Ltd. R305
 Current Biology

Dispatches

which they create for the developing In their recent study, Chen et al. [1] show happening at a distance where the visual-
organism are significant. The crossmodal that visual experience is also crucial to the to-auditory lag would be at all significant.
binding problem [3,4] threatens adults’ and typical development of multisensory It seems more likely that the auditory-to-
infants’ ability to perceive a coherent simultaneity perception. Presenting visual lags due to differences in the speed
multisensory world: Coherent multisensory audiovisual stimuli with a range of onset of auditory and visual neural transduction
perception of timing is threatened by asynchronies they asked adult to the central nervous system, which are
temporal asynchrony introduced by participants to judge whether or not the close to 45 ms in the adult, would be a
differences in neural transduction between auditory and visual components occurred more pertinent concern for crossmodal
the senses (e.g., vision takes about simultaneously. Participants who had had temporal calibration at this age.
45 ms longer than sound to reach the congenital cataracts in both eyes in early Interestingly, this 45 ms crossmodal
central nervous system [3]). Coherent infancy (up to about 4 months of age) transduction differential is quite close to
multisensory perception of space is showed an atypical pattern of simultaneity the visual-auditory lag at which Chen
threatened by the fact that the brain codes perception; they were biased to judge et al.’s visually deprived participants
spatial position in different ways across the visual-leading events as simultaneous. demonstrated their point of subjective
senses (e.g., visual location is coded in Their point of subjective simultaneity for simultaneity. So perhaps the effect of
retinocentric coordinates, and tactile such events was where the visual stimulus audiovisual deprivation in the first months
location in somatosensory coordinates, led the auditory stimulus by 43 ms. of life is that it prevents infants from
and the transformations between visual, Interestingly, no such atypical partialing out the lags between auditory
auditory and tactile codes depend on the development was seen when the same and visual signals due to crossmodal
relative postures of eyes, ears, and limbs, participants were asked to judge visual- transduction differentials. And so this
which change frequently [5,6]). But the tactile simultaneity. On this basis Chen might explain why these infants later, as
crossmodal binding problem is not et al. make an important point: effects of adults, perceive events where the visual
purely biological: Even before physical visual deprivation are not just visual. Visual stimulus precedes the auditory stimulus as
information has reached our sensory deprivation in infancy also deprived these being simultaneous. But then why should
apparatus, differences in the physics of individuals of the multisensory visual-tactile simultaneity not also be
the different media of transmission (e.g., experiences which they need in order to affected by the corresponding deprivation
sound waves, pulses of electromagnetic develop a typical sense of audiovisual of visual-tactile experience? Again, I think
radiation, the diffusion of chemicals) give timing. But what are these multisensory the answer lies in a consideration of the
rise to asynchronies and dislocations experiences and how do they influence newborn multisensory experience.
across those media. multisensory development?
So how do our central nervous systems Visual-tactile Experiences in the First
learn to abstract a coherent world from Audiovisual Experiences in the First Months of Life
this multisensory mess (or ‘‘sensory Months of Life It is surprising how little visual regard
bouillabaisse’’ according to one of the Newborn human babies do not live in newborn infants have for their own bodies.
authors of [1])? We now know a lot about the same multisensory milieu as adults. Visual orienting to tactile stimuli is not
how adults solve the ‘‘crossmodal binding Altricial and myopic, they depend on behaviourally robust until around
problem’’ (e.g., [3,4,7,8]), but there has focuses of attention and interest (people, 10 months of age [13]. Even when they start
been remarkably little consideration of the faces, hands) [12] being brought to them reaching for objects, they tend to be just as
origins of such solutions in developmental (or vice versa). It would be very odd to see successful in the light as in the dark
psychology. This is odd, because an adult talking to a newborn from across (indicating that visual control of the hand is
the various threats to multisensory a room. As caregivers, we tend to get up not important [14]). We also know that at
perception discussed above change close to provide young babies with a 4 months of age infants do not refer
dramatically in their nature and impact rich, nearby — almost peripersonal — vibrotactile stimuli on their feet to a location
across early life, requiring continual multisensory environment. in external (visual) space [15]. So perhaps
recalibrations [9]. Perhaps the most The up-close-and-personal audiovisual this is why Chen et al.’s participants
revealing studies to date come from environment of the newborn is why I doubt showed no atypical development of visual-
research involving participants with visual one of Chen et al.’s [1] explanations for their tactile simultaneity judgments. Because
deprivation early in life. In the domain of findings. They suggest that the specific their sight was restored at around
multisensory space, studies indicate the effect of visual deprivation on audiovisual 4.5 months, they were only deprived of
importance of visual experience in early simultaneity perception (and not visual- visual-tactile experience in a period in
development. The most recent case tactile simultaneity) may be due to the fact which infants do not spend much time
studies of congenitally blind individuals that infants have to calibrate audiovisual considering such multisensory content in
who have had their sight restored through simultaneity under conditions of visual- any case. This would seem to chime with a
the removal of cataracts seems to to-auditory lag given the slower transit recent study [10] which indicates that visual
indicate that deprivation of vision in a of sound-waves towards the observer deprivation in the first five months
sensitive period between 5 months [10] (visual-tactile events only occur in near of life does not impair the typical
and two years [11] leads to atypical space). But I can’t think of many instances development of tactile spatial perception
development of an ability to map touches in which infants younger than 5 months as it does when such deprivation continues
into visual space. would be interested in audiovisual events into later infancy [11] and childhood.

R306 Current Biology 27, R294–R317, April 24, 2017

Dispatches

The Development of Multisensory 6. Jay, M.F., and Sparks, D.L. (1984). Auditory 13. Fausey, C.M., Jayaraman, S., and Smith, L.B.
receptive fields in primate superior colliculus (2016). From faces to hands: Changing visual
Timing Beyond Early Infancy shift with changes in eye position. Nature 309, input in the first two years. Cognition 152,
In this dispatch, I have suggested that 345–347. 101–107.
the sensorimotor and perceptual
7. Sugita, Y., and Suzuki, Y. (2003). Audiovisual 14. Bremner, A.J., Mareschal, D., Lloyd-Fox, S.,
limitations of the newborn infant place perception: Implicit estimation of sound-arrival and Spence, C. (2008). Spatial localization of
certain constraints on the ways in which time. Nature 421, 911–911. touch in the first year of life: Early influence of a
they experience and learn from their visual spatial code and the development of
8. Kopinska, A., and Harris, L.R. (2004).
remapping across changes in limb position.
multisensory environment. But of course in Simultaneity constancy. Perception 33,
J. Exp. Psychol. Gen. 137, 149–162.
the second half year of life, typically 1049–1060.

developing infants increasingly take a 9. Burr, D., Binda, P., and Gori, M. (2011). 15. Bremner, A.J., Holmes, N.P., and Spence, C.
Multisensory integration and calibration in (2008). Infants lost in (peripersonal) space?
more active interest in their environment,
adults and in children. In Sensory Cue Trends Cogn. Sci. 12, 298–305.
starting to make their first successful Integration, J. Trommershauser, K. Kording,
grasps for objects, and later still beginning and M.S. Landy, eds. (Oxford, UK: Oxford 16. Begum Ali, J.B., Spence, C., and Bremner, A.J.
to locomote around their environments University Press), pp. 173–194. (2015). Human infants’ ability to perceive touch
in external space develops postnatally. Curr.
towards more distant goals [12]. These 10. Azañón, E., Camacho, K., Morales, M., and Biol. 25, R978–R979.
sensorimotor developments bring about Longo, M.R. (2017). The sensitive period for
tactile remapping does not include early 17. Chen, Y.C., Shore, D.I., Lewis, T.L., and
new multisensory experiences which lead infancy. Child Dev., in press. Maurer, D. (2016). The development of the
to new complications of the crossmodal perception of audiovisual simultaneity. J. Exp.
11. Ley, P., Bottari, D., Shenoy, B.H., Kekunnaya,
binding problem. For instance, as infants Child Psychol. 146, 17–33.
R., and Röder, B. (2013). Partial recovery of
begin to deal with a wider repertoire of visual–spatial remapping of touch after
restoring vision in a congenitally blind man. 18. Lewkowicz, D.J. (1996). Perception of
different scales of spatial environment, auditory–visual temporal synchrony in human
Neuropsychologia 51, 1119–1123.
they will have to cope with similarly varying infants. J. Exp. Psychol. Human Percept.
temporal lags between visual and auditory 12. Adolph, K.E., and Berger, S.E. (2015). Physical Perform. 22, 1094–1106.
and motor development. In Developmental
stimuli arising from the same external Science: An Advanced Textbook, 7th ed., M.H. 19. Lewkowicz, D.J., and Flom, R. (2014). The
events and develop the kinds Bornstein, and M.E. Lamb, eds. (New York: audiovisual temporal binding window narrows
of compensatory mechanisms which Psychology Press), pp. 261–333. in early childhood. Child Dev. 85, 685–694.
adults use in such circumstances [3,7,8].
Maybe this is what made it difficult for
Chen et al.’s participants to recalibrate
audiovisual simultaneity after their
sight was restored at 4 months. For
both typically and atypically developing
children, it probably makes a bit of sense in
these temporally variable multisensory Gut Microbiota: Small Molecules
circumstances to bind stimuli together
across a wider temporal window, and such Modulate Host Cellular Functions
wider temporal windows of crossmodal
binding have been observed several times Jacob M. Luber1,2,3,4,* and Aleksandar D. Kostic1,2,4,*
1Section on Pathophysiology and Molecular Pharmacology, Joslin Diabetes Center, Boston,
now in infants and children [16–19].
MA 02215, USA
2Section on Islet Cell and Regenerative Biology, Joslin Diabetes Center, Boston, MA 02215,
REFERENCES
USA
3Division of Medical Sciences, Harvard Medical School, Boston, MA 02115, USA
1. Chen, Y.-C., Lewis, T.L., Shore, D.I., and 4Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA
Maurer, D. (2017). Early binocular input is
critical for development of audiovisual but not 02115, USA
visualtactile simultaneity perception. Curr. Biol. *Correspondence: [email protected] (J.M.L.), [email protected]
27, 583–589. (A.D.K.)
2. Stein, B.E., ed. (2012). The New Handbook of http://dx.doi.org/10.1016/j.cub.2017.03.026
Multisensory Processing (Cambridge, MA: MIT
Press).
The human gut metagenome was recently discovered to encode vast
3. Harris, L.R., Harrar, V., Jaekl, P., and Kopinska, collections of biosynthetic gene clusters with diverse chemical
A. (2010). Mechanisms of simultaneity
constancy. In Space and Time in Perception potential, almost none of which are yet functionally validated. Recent
and Action, R. Nijhawan, ed. (Cambridge, UK: work elucidates common microbiome-derived biosynthetic gene
Cambridge University Press), pp. 232–253.
clusters encoding peptide aldehydes that inhibit human proteases.
4. Körding, K.P., Beierholm, U., Ma, W.J., Quartz,
S., Tenenbaum, J.B., and Shams, L. (2007).
Causal inference in multisensory perception.
PLoS One 2, e943. Biosynthetic gene clusters (BGCs) are products without cellular machinery such
tightly clustered groups of genes in as ribosomes [1]. The array of diverse
5. Bremner, A.J., and van Velzen, J. (2015).
Sensorimotor control: Retuning the body– bacteria that encode pathways capable of natural products produced by BGCs is
world interface. Curr. Biol. 25, R159–R161. producing small-molecule natural vast; current databases hold more than

Current Biology 27, R294–R317, April 24, 2017 ª 2017 Elsevier Ltd. R307