Translation-Invariant Orientation Tuning in Visual “Complex” Cells Could Derive from Intradendritic Computations

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.