Neurons in the primary visual cortex are selective for the size, orientation and direction of motion of patterns falling within a restricted region of visual space known as the receptive field. The response to stimuli presented within the receptive field can be facilitated or suppressed by other stimuli falling outside the receptive field which, when presented in isolation, fail to activate the cell. Whether this interaction is facilitative or suppressive depends on the relative orientation of pattern elements inside and outside the receptive field. Here we show that neuronal facilitation preferentially occurs when a near-threshold stimulus inside the receptive field is flanked by higher-contrast, collinear elements located in surrounding regions of visual space. Collinear flanks and orthogonally oriented flanks, however, both act to reduce the response to high-contrast stimuli presented within the receptive field. The observed pattern of facilitation and suppression may be the cellular basis for the observation in humans that the detectability of an oriented pattern is enhanced by collinear flanking elements. Modulation of neuronal responses by stimuli falling outside their receptive fields may thus represent an early neural mechanism for encoding objects and enhancing their perceptual saliency.

Visual stimulation of a region outside the receptive field of single cells in visual cortex often results in the modulation of their responses. The modulatory effects are thought to be mediated through lateral connections within visual cortex. Research on lateral interactions commonly shows suppression. There has been no systematic study of the optimal conditions for facilitation. Here we have studied the nature of the modulation using a new type of compound stimulus: contrast reversal of pattern stimuli made of three discrete grating patches. The middle patch, optimally fitted to the receptive field in orientation, size, and spatial as well as temporal frequencies, was flanked by two similar patches presented well outside the receptive field. We found that (1) both facilitation and suppression occurred often in the same cells, when orientations of the target and flankers matched the receptive-field's optimal orientation; (2) facilitation with collinear flankers occurred most frequently at target contrasts just above the cell's firing threshold and suppression prevailed at high contrasts; (3) facilitative or suppressive modulation was obtained with target-flankers separation of up to 12 deg or more; (4) collinear facilitation was lost when flankers' orientation was rotated by 90 deg, while keeping all other parameters the same; and (5) neither the modulation mode nor the proportion of modulated cells was related to the cell types (simple vs. complex cells) and cells' laminar locations. Here we have provided physiological evidence for contrast-dependent, collinear facilitation probably underlying perceptual grouping in humans.

Single-cell responses in visual cortex to a target falling within their receptive field can be modified by collinear flanking stimuli concurrently presented outside the receptive field. Here, we report the presence of four types of contrast-dependent lateral effects: (1) facilitation at low target contrasts and suppression at high contrasts, (2) facilitation that increases with contrast, (3) suppression that increases with contrast, and (4) suppression at low contrasts with facilitation at high contrasts. We propose a sensitivity modulation model that accounts for all the four types of lateral effects by changes in two parameters. In this model, activation of neighboring neurons changes the sensitivities of the target neuron to both the direct feedforward input and inhibitory, divisive feedback from neighboring neurons.

Monocularly deprived kittens were compared with littermates that had had their eyelids sutured for the same time but that had, in addition, been treated with 6-hydroxydopamine to deplete their forebrains of catecholamines. The visual cortices of all the catecholamine-depleted kittens showed high proportions of binocular neurons, in contrast to the control group, most of whose visual cortical neurons were driven exclusively by the nondeprived eye. Catecholamines may play an important role in the maintenance of cortical plasticity during the critical period.

Using a newly developed technique of continuous microperfusion, we obtained further evidence in support of our hypothesis that the neocortical catecholamines (CAs), particularly norepinephrine (NE), are responsible for a high level of cortical plasticity. We used the visual cortical changes in ocular dominance which follow a brief monocular deprivation as a simple and reliable index of cortical plasticity. Local perfusion of kitten visual cortex with 1 mg/ml (4.0 mM) 6-hydroxydopamine (6-OHDA) prevented the effects of monocular deprivation in kittens, thus replicating the results we had obtained using intraventricular injections (Kasamatsu and Pettigrew, '76b, '79). Locally perfused NE at a concentration of of 10(-2) mg/ml (48.6 micron) restored visual cortical plasticity in animals which were no longer susceptible to brief monocular lid-suture. These numbers refer to the concentration of solutions in the cannula/minipump system. The effective concentrations at the site of recording (about 2 mm away) are probably much lower than these. This effect of NE perfusion was seen both in kittens which had received prior 6-OHDA treatment as well as in older animals which had outgrown the susceptible period. In the kittens we obtained as a nearly complete shift in ocular dominance toward the open eye and in the older animals a decrease in binocularity was obtained. The changes were found only in the local region of visual cortex perfused with either NE or 6-OHDA, while nearby cortical regions in the same animals were unaffected. There were no obvious changes in receptive field properties of individual neurons other than ocularity, and externally perfused NE did not itself reduce binocularity in normal animals: the effects of NE described about only occurred when the animal's visual experience was simultaneously altered. These results support the view that NE plays an important role in cortical plasticity.