Journal of Neuroscience, Vol 14, 7291-7305, Copyright © 1994 by Society for Neuroscience
Functional mapping of horizontal connections in developing ferret visual cortex: experiments and modeling
M Weliky and LC Katz
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710.
In cat striate cortex, patchy horizontal axonal projections link columns of
similar orientation specificity. To assess the physiological correlates of
such clustered projections, a new multisite stimulation technique was used
to functionally map the pattern of horizontal synaptic inputs onto single
layer 2/3 cells within tangential slices of developing ferret visual
cortex. Twenty-four separate sets of horizontal fibers were stimulated
within a 1200 microns strip of cortex, while evoked synaptic responses were
recorded using whole-cell patch methods. For most cells, input maps
demonstrated the presence of clustered horizontal connections in which
multiple strong and weak synaptic responses were alternately evoked across
the stimulated cortical region. Recordings from up to nine cells in a
single slice revealed that patterns of synaptic input were closely
correlated for cells in close proximity, and that this correlation
decreased with distance, with no correlation at distances greater than 500
microns. To determine whether these physiological results were consistent
with the known anatomical linkage of iso-orientation columns by clustered
horizontal connections, mathematical analysis and computer simulations were
performed upon orientation tuning maps obtained from optical imaging of
activity-dependent intrinsic signals in mature ferret visual cortex.
Optical imaging revealed an organization of iso-orientation domains
consisting of broad regions of cortex across which orientation preference
smoothly varied, together with "orientation centers" around which
orientation preference was arranged in a pinwheel manner. The distribution
of synaptic connections between different cortical sites was simulated by a
model of functionally linked iso- orientation columns. Simulated synaptic
input maps, generated by the same stimulation and recording arrangements
used in our experimental protocol, accurately reproduced the observed
patterns of clustered inputs onto experimentally recorded cells. These
results indicate that even at the time of eye opening, prior to extensive
visual experience, most cells receive patterns of synaptic inputs
consistent with a clustered organization of horizontal connections that
functionally link iso-orientation columns.
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