Developmental reorganisation of visual motion pathwaysJohn Wattam-Bell, Melissa Chiu & Louisa Kulke

Visual Development Unit, Dept. of Developmental Science, Division of Psychology & Language Sciences, UCL

Globally coherent visual motion activates a network of extrastriate cortical areas, including V5/MT+, V3a and V61. Little is known about the development of this network.

Recent evidence from steady-state event-related potentials (ERPs) to motion coherence indicates a substantial reorganisation of the network between infancy and adulthood2.

Steady-state ERPs give a sensitive measure of cortical responses, but confound timing and polarity information that could shed light on the nature of the reorganisation. To address this, we have measured transient ERPs to the onset of coherent and incoherent motion in infants and adults. The results suggest that emergence of feedback from extrastriate cortex to V1/V2 may play a key role in the developmental reorganisation of the motion pathways.

1. Braddick et al (2001) Perception 30, 61; Pitzalis et al (2010) Cerebral Cortex 20, 4112. Wattam-Bell et al (2010) Current Biology 20,4113. Maris & Oostenveld (2007) J. Neurosci. Methods 164, 1774. Stillito et al (2006) TINS 29, 3075. Huttenlocher (1982) Neuroscience Letters 33,2476. Burkhalter (1993) Cerebral Cortex 3, 4767. Tadel et al (2011) Computational Intelligence and Neuroscience, vol. 2011, ID 879716

Introduction

The coherence ERP is the differential response to the two levels of coherence - ie a global response, requiring integration of local motion information.

Adult subjects

Posterior ERP components labelled in the figure above:A: bilateral negative components from ~160 msec, consistent with V5/MT+ activationB: midline positive component from ~200 msec, consistent with a V1/V2 origin.

Feedforward responses in V1/V2 are not expected to show differential sensitivity to coherence, which is a global stimulus property. Global responses in these areas are probably driven by feedback from extrastriate areas4. The relative timing of the V5/MT+ and V1/V2 ERP components is consistent with this.

Infant subjectsThe infants showed no real evidence of a coherence response. This is probably due to the low signal-to-noise ratio of transient ERPs; the more sensitive steady-state technique gives clear evidence for differential responses to motion coherence at these ages3.

The cortical activations displayed on the right show absolute values of ERP source strength

Adult subjects

A: positive component (V1/V2), spreading laterally (V3a?) before switching at 180 msec toB: negative component from V1/V2 which dominates the rest of the ERP (C). This

component may reflect feedback from extrastriate cortex to V1/V2

Infants 3-5 months

Starts similarly to adult ERP (A: V1/V2, spreading laterally), but no abrupt switch. Instead, the spread continues to distinct lateral foci (B) with sources in V5/MT+. This infant ERP may reflect purely forward activation, without the feedback from extrastriate cortex to V1/V2 that seems to dominate the ERP in adults.

Infants 6-9 months

A: 158 msec

C: 398 msec

A: 118 msec

B: 398 msec

C: 278 msec

ERPs were recorded with a 128-channel EGI geodesic system

Subjects•13 adults, aged 18-36 years•21 infants; infants were tested twice, first at 3-5 months of age, then

at 6-9 months

Stimulus• random-dot kinematogram, 2000 dots, dot size 0.2 deg, area 35 x 26 deg•coherent motion: dots moved along circular trajectories at 6.1 deg/sec (linear speed)• incoherent motion: dots moved in random directions at 6.1 deg/sec

ERP trials•moving stimulus presented in 0.8 sec trials• random inter-trial interval (1.2 - 3 sec) with static dots•coherent and incoherent motion trials randomly

interleaved

ERP processing and analysisIndividual data• filtering: 0.2 - 30 Hz (3rd order zero-phase filters)•epoching: -200 to 800 msec relative to trial onsets•artifact rejection, baseline correction, average reference•epoch averaging: separate averages for coherent and incoherent motion trials

Group analysis•The individual coherent and incoherent averages were combined in two ways:▪ motion coherence ERP = coherent response - incoherent response. Differential

response to the two levels of coherence, 0% & 100%.▪ motion onset ERP = coherent response + incoherent response. Response to onset of

motion in an initially static pattern.ERP components were defined as the space-time connected regions of positive or negative scalp potential that emerge from thresholding the signal above and below the baseline3. Component significance was assessed with a randomization test3. Unless otherwise stated, the components discussed here were significant at p<0.05, corrected for FWE. Brainstorm7 was used to estimate the cortical sources of the ERPs, based on nominal (ie not measured) electrode positions, coregistered to a standard adult head (MNI Colin27).

inter-trialinterval

coherentmotion trial

incoherentmotion trial

inter-trial interval

Methods

Results 1: motion coherence ERP

Results 2: motion onset ERP

In the mature visual system, cortical feedback produces contextual (extra-classical) effects4, allowing global information to modulate activity in local areas such as V1/V2. This feedback probably underlies the late onset V1/V2 components that dominate the adult ERP.

The absence of these components in younger infants suggests that emergence of cortical feedback might be a major factor in the developmental reorganisation of cortical motion processing.

This is consistent with the well-known pattern of rapid proliferation of cortical synapses in the first months of life, followed by gradual pruning throughout childhood5. This pattern is largely confined to lateral and feedback connections6, which implies that these connections are the main site of developmental cortical plasticity.

During the phase of synaptic proliferation, newly-formed connections are presumably quite random, with limited functionality; it is probably the subsequent pruning that imposes functional order. Interestingly, the transition between these two phases occurs at about 7-8 months, around the time when the first hint of feedback is seen in our ERP data.

Discussion

References

The 6-9 month ERP is very similar to that at 3-5 months. However, there is an additional (but not significant: p=0.09) negative midline component (C), as seen in adults but not at 3-5 months – the first hint of emerging feedback to V1/V2?

Group average ERP across all channels, from stimulus onset at time=0

Topographic plots of scalp potential at indicated times. Front of head at top. Red = positive blue = negative.

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