Models of receptive-field dynamics in visual cortex

Abstract

The position, size, and shape of the receptive field (RF) of some cortical neurons change dynamically, in response to artificial scotoma conditioning (Pettet & Gilbert, 1992) and to retinal lesions (Chino et al., 1992; Darian-Smith & Gilbert, 1995) in adult animals. The RF dynamics are of interest because they show how visual systems may adaptively overcome damage (from lesions, scotomas, or other failures), may enhance processing efficiency by altering RF coverage in response to visual demand, and may perform perceptual learning. This paper presents an afferent excitatory synaptic plasticity rule and a lateral inhibitory synaptic plasticity rule--the EXIN rules (Marshall, 1995)--to model persistent RF changes after artificial scotoma conditioning and retinal lesions. The EXIN model is compared to the LISSOM model (Sirosh et al., 1996) and to a neuronal adaptation model (Xing & Gerstein, 1994). The rules within each model are isolated and are analyzed independently, to elucidate their roles in adult cortical RF dynamics. Based on computer simulations, the EXIN lateral inhibitory synaptic plasticity rule and the LISSOM lateral excitatory synaptic plasticity rule produced the best fit with current neurophysiological data on visual cortical plasticity in adult animals (Chino et al., 1992; Pettet & Gilbert, 1992; Darian-Smith & Gilbert, 1995) including (1) the retinal position and shape of the expanding RFs; (2) the corticotopic direction in which responsiveness returns to the silenced cortex; (3) the direction of RF shifts; (4) the amount of change in response to blank stimuli; and (5) the lack of dynamic RF changes during conditioning with a retinal lesion in one eye and the unlesioned eye kept open, in adult animals. The effects of the LISSOM lateral inhibitory synaptic plasticity rule during artificial scotoma conditioning are in conflict with those of the other two LISSOM synaptic plasticity rules. A novel "complementary scotoma" conditioning experiment, in which stimulation of two complementary regions of visual space alternates repeatedly, is proposed to differentiate the predictions of the EXIN and LISSOM rules.

Hyper-vision in a patient with central and paracentral vision loss reflects cortical reorganization

“…The outcome is either relative response gain or receptive-field expansion of neurons inside the scotoma rendering them selective to stimulation around the receptive field. Simulation studies also support the suggestion that cortical neurons selective to visual stimuli in the area of the visual field corresponding to the retinal lesion may become selective to other parts of the visual field (Xing & Gerstein, 1994;Kalarickal & Marshall, 1999, 2002Xing & Heeger, 2000;Andrade et al, 2001). If similar plasticity effects occurred in patients with central scotoma, they would probably lead to a relative modification in filtering properties of neurons in silenced cortical area, or else to a relative response gain.…”

“…In support of this suggestion, Braun et al (2001) showed that lesions in the peripheral visual system induce disinhibition due to changes in intracortical connectivity, resulting in increased cortical activity. Simulation studies also support the suggestion that cortical neurons selective to visual stimuli in the area of the visual field corresponding to the retinal lesion may become selective to other parts of the visual field (Xing & Gerstein, 1994;Kalarickal & Marshall, 1999, 2002Xing & Heeger, 2000;Andrade et al, 2001). The outcome is either relative response gain or receptive-field expansion of neurons inside the scotoma rendering them selective to stimulation around the receptive field.…”

Role of Synaptic and Intrinsic Membrane Properties in Short-Term Receptive Field Dynamics in Cat Area 17

“…Previous hypotheses to explain RF dynamics have proposed an adaptation of surround inhibition or a potentiation of horizontal connections by the prolonged scotoma presentation (Pettet and Gilbert, 1992;Xing and Gerstein, 1994;DeAngelis et al, 1995;Kalarickal and Marshall, 1999;Cavanaugh et al, 2002). Our results offer an alternative explanation, which is based on the adaptation state of the cells before RF measurements.…”

Rearrangement of receptive field topography after intracortical and peripheral stimulation: the role of plasticity in inhibitory pathways

“…The EXIN lateral inhibitory synaptic plasticity models dynamic RF changes produced by artificial scotoma conditioning and retinal lesions (Kalarickal andMarshall 1999, Marshall andKalarickal 1997). The EXIN rules have been used to model development of disparity selectivity (Marshall 1990c), motion selectivity and grouping (Marshall 1990a, 1995b, Schmitt and Marshall 1995, orientation selectivity (Marshall 1990d) and length selectivity and end-stopping (Marshall 1990b).…”