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The Journal of Neuroscience, June 1, 1998, 18(11):4325-4334
Translation-Invariant Orientation Tuning in Visual "Complex"
Cells Could Derive from Intradendritic Computations
Bartlett W.
Mel1,
Daniel L.
Ruderman1, and
Kevin A.
Archie2
1 Department of Biomedical Engineering and
2 Neuroscience Program, University of Southern California,
Los Angeles, California 90089
Hubel and Wiesel (1962) first distinguished "simple" from
"complex" cells in visual cortex and proposed a processing
hierarchy in which rows of LGN cells are pooled to drive oriented
simple cell subunits, which are pooled in turn to drive complex cells. Although parsimonious and highly influential, the pure hierarchical model has since been challenged by results indicating that many complex
cells receive excitatory monosynaptic input from LGN cells or do not
depend on simple cell input. Alternative accounts of complex cell
orientation tuning remain scant, however, and the function of
monosynaptic LGN contacts onto complex cell dendrites remains unknown.
We have used a biophysically detailed compartmental model to
investigate whether nonlinear integration of LGN synaptic inputs within
the dendrites of individual pyramidal cells could contribute to
complex-cell receptive field structure. We show that an isolated
cortical neuron with "active" dendrites, driven only by excitatory
inputs from overlapping ON- and OFF-center LGN subfields, can produce
clear phase-invariant orientation tuning a hallmark response
characteristic of a complex cell. The tuning is shown to depend
critically both on the spatial arrangement of LGN synaptic contacts
across the complex cell dendritic tree, established by a Hebbian
developmental principle, and on the physiological efficacy of
excitatory voltage-dependent dendritic ion channels. We conclude that
unoriented LGN inputs to a complex cell could contribute in a
significant way to its orientation tuning, acting in concert with
oriented inputs to the same cell provided by simple cells or other
complex cells. As such, our model provides a novel, experimentally
testable hypothesis regarding the basis of orientation tuning in the
complex cell population, and more generally underscores the potential
importance of nonlinear intradendritic subunit processing in cortical
neurophysiology.
Key words:
complex cells; orientation tuning; active dendrites; single neuron computation; visual cortex; energy models; computational
models
Copyright © 1998 Society for Neuroscience 0270-6474/98/18114325-10$05.00/0
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