Contrast-Invariant Orientation Tuning in Cat Visual Cortex: Thalamocortical Input Tuning and Correlation-Based Intracortical Connectivity

Abstract

The origin of orientation selectivity in visual cortical responses is a central problem for understanding cerebral cortical circuitry. In cats, many experiments suggest that orientation selectivity arises from the arrangement of lateral geniculate nucleus (LGN) afferents to layer 4 simple cells. However, this explanation is not sufficient to account for the contrast invariance of orientation tuning. To understand contrast invariance, we first characterize the input to cat simple cells generated by the oriented arrangement of LGN afferents. We demonstrate that it has two components: a spatial-phase-specific component (i.e., one that depends on receptive field spatial phase), which is tuned for orientation, and a phase-nonspecific component, which is untuned. Both components grow with contrast. Second, we show that a correlation-based intracortical circuit, in which connectivity between cell pairs is determined by the correlation of their LGN inputs, is sufficient to achieve well tuned, contrast-invariant orientation tuning. This circuit generates both spatially opponent, "antiphase" inhibition ("push-pull"), and spatially matched, "same-phase" excitation. The inhibition, if sufficiently strong, suppresses the untuned input component and sharpens responses to the tuned component at all contrasts. The excitation amplifies tuned responses. This circuit agrees with experimental evidence showing spatial opponency between, and similar orientation tuning of, the excitatory and inhibitory inputs received by a simple cell. Orientation tuning is primarily input driven, accounting for the observed invariance of tuning width after removal of intracortical synaptic input, as well as for the dependence of orientation tuning on stimulus spatial frequency. The model differs from previous push-pull models in requiring dominant rather than balanced inhibition and in predicting that a population of layer 4 inhibitory neurons should respond in a contrast-dependent manner to stimuli of all orientations, although their tuning width may be similar to that of excitatory neurons. The model demonstrates that fundamental response properties of cortical layer 4 can be explained by circuitry expected to develop under correlation-based rules of synaptic plasticity, and shows how such circuitry allows the cortex to distinguish stimulus intensity from stimulus form.

Learning and Adaptation in a Recurrent Model of V1 Orientation Selectivity

“…However, other problems with the recurrent model, such as the inconsistency with the cortical inactivation experiments and the near independence of tuning on stimulus' spatial frequency, have been noted (Ferster and Miller 2000) and have prompted Troyer et al (1998) to propose a modified feed-forward model. According to this model, V1 orientation tuning mainly results from the feed-forward mechanism and the contrast invariance is maintained by feed-forward inhibition between cells with opposite receptive field polarities.…”

“…According to this model, V1 orientation tuning mainly results from the feed-forward mechanism and the contrast invariance is maintained by feed-forward inhibition between cells with opposite receptive field polarities. While successful in many ways (Kayser et al 2001;Krukowski and Miller 2001;Troyer et al 1998), the modified model is unlikely to explain the learning-and adaptation-induced changes because it does not assume a Mexican-hat interaction profile among cells tuned to different orientations. It is also not clear if the modified feedforward model is consistent with some other phenomena accounted for by the recurrent model (Somers et al 1995;Sompolinsky and Shapley 1997).…”

Local networks in visual cortex and their influence on neuronal responses and dynamics

“…The DC component is the part of the response that is not specific for spatial phase of the stimulus. This raises the possibility that the local circuit contribution to the subthreshold response is not phase selective, as proposed in some models of cortical circuits [43], but not others [67]. It is also possible that the orientation map used to calculate the local input tuning is based on slow intrinsic signals that do not provide information about stimulus phase.…”

A minimal mechanistic model for temporal signal processing in the lateral geniculate nucleus

“…A common choice of firing rate functions F r (x) for LGN neurons has been the half-wave rectification function (Gazères et al 1998;Troyer et al 1998Troyer et al , 2002Einevoll and Heggelund 2000), but sigmoidal functions have also been used (Hayot and Tranchina 2001;Yousif and Denham 2007). For now we leave F r ON (x), as well as the other firing-rate functions introduced below, unspecified.…”

“…We now assume the firing-rate functions of both the LGN and cortical cells to be half-wave rectifying functions (Gazères et al 1998;Troyer et al 1998Troyer et al , 2002Einevoll and Heggelund 2000;Dayan and Abbott 2001), i.e.,…”