Distinct spatiotemporal mechanisms underlie extra-classical receptive field modulation in macaque V1 microcircuits

Abstract

Complex scene perception depends upon the interaction between signals from the classical receptive field (CRF) and the extra-classical receptive field (eCRF) in primary visual cortex (V1) neurons. Although much is known about V1 eCRF properties, we do not yet know how the underlying mechanisms map onto the cortical microcircuit. We probed the spatio-temporal dynamics of eCRF modulation using a reverse correlation paradigm, and found three principal eCRF mechanisms: tuned-facilitation, untuned-suppression, and tuned-suppression. Each mechanism had a distinct timing and spatial profile. Laminar analysis showed that the timing, orientation-tuning, and strength of eCRF mechanisms had distinct signatures within magnocellular and parvocellular processing streams in the V1 microcircuit. The existence of multiple eCRF mechanisms provides new insights into how V1 responds to spatial context. Modeling revealed that the differences in timing and scale of these mechanisms predicted distinct patterns of net modulation, reconciling many previous disparate physiological and psychophysical findings.

Surround Modulation Properties of Tectal Neurons in Pigeons Characterized by Moving and Flashed Stimuli

“…Taken together, visual neurons in both avian OT and the preliminary stages of the visual system of mammals, including retina [ 63 , 64 , 65 , 66 ], SC [ 22 , 67 ], LGN [ 33 , 68 ] and V1 [ 32 , 69 , 70 ], have similar RF structures, most of which presented a concentric organization characterized by an excitatory CRF surrounded by an inhibitory eCRF. The main difference between birds and mammals is that most V1 neurons are orientation selective which means that they respond best to particular orientation stimuli but not to the orthogonal orientation [ 71 ].…”

“…The surround modulation properties reported in mammals are almost related to the nature of neurons, which are selective to orientation or spatial frequency [ 22 , 32 , 33 ]. In avians, neurons in OT mostly respond to motion [ 34 , 35 ] or change in luminance [ 36 , 37 ].…”

Neural Correlates of Perceptual Similarity Masking in Primate V1

“…The nature of contextual modulations in V1 is quite complex (Angelucci et al 2017, Angelucci & Bressloff 2006, Bai et al 2021, Cavanaugh et al 2002b, Henry et al 2020, Michel et al 2018, Polat et al 1998, Sceniak et al 1999, Shushruth et al 2012). A second goal of our study was to quantitatively characterize the spatiotemporal dynamics of columnar-scale V1 population responses to targets and backgrounds of different orientations and contrasts.…”

“…The responses of visual neurons to a target can be strongly modulated by the context in which the stimulus is presented. Such contextual modulations have powerful, complex and diverse effects in the visual cortex (Allman et al 1985, Angelucci et al 2017, Angelucci & Bressloff 2006, Bai et al 2021, Cavanaugh et al 2002b, Henry et al 2020, Michel et al 2018, Sceniak et al 1999, Shushruth et al 2012). Most of these effects reflect sublinear interactions between the target and the background, suggesting that they could potentially contribute to behavioral masking effects.…”

Foundations of visual form selectivity for neurons in macaque V1 and V2

“…Second, these approaches have used rapid sequential stimulus presentations to estimate a neuron’s receptive field in space and time [8, 31]. Given the dynamic selectivity of V1 neurons[25, 35], particularly over the extra-classical receptive field [7, 17, 38, 43, 52], it is unclear whether V2 response patterns measured using rapidly changing stimuli will extrapolate to more natural viewing conditions. Finally, interpreting model fits can be difficult when filters in intermediate layers do not cleanly map to earlier levels of neural processing [5].…”