Spatiotemporal characteristics of surround suppression in primary visual cortex and lateral geniculate nucleus of the cat

Abstract

In the primary visual cortex (V1), a neuronal response to stimulation of the classical receptive field (CRF) is predominantly suppressed by a stimulus presented outside the CRF (extraclassical receptive field, ECRF), a phenomenon referred to as ECRF suppression. To elucidate the neuronal mechanisms and origin of ECRF suppression in V1 of anesthetized cats, we examined the temporal properties of the spatial extent and orientation specificity of ECRF suppression in V1 and the lateral geniculate nucleus (LGN), using stationary-flashed sinusoidal grating. In V1, we found three components of ECRF suppression: (1) local and fast, (2) global and fast, and (3) global and late. The local and fast component, which resulted from within 2° of the boundary of the CRF, started no more than 10 ms after the onset of the CRF response and exhibited low specificity for the orientation of the ECRF stimulus. These spatiotemporal properties corresponded to those of geniculate ECRF suppression, suggesting that the local and fast component of V1 is inherited from the LGN. In contrast, the two global components showed rather large spatial extents ∼5° from the CRF boundary and high specificity for orientation, suggesting that their possible origin is the cortex, not the LGN. Correspondingly, the local component was observed in all neurons of the thalamocortical recipient layer, while the global component was biased toward other layers. Therefore, we conclude that both subcortical and cortical mechanisms with different spatiotemporal properties are involved in ECRF suppression.

Dynamic tilt illusion induced by continuous contextual orientation alternations

“…Researchers manipulating the temporal separation between the center patch and the oriented context found that, although the tilt illusion decreases as the stimulus onset asynchrony increases, it completely disappears only when the context precedes the center beyond about 300 ms (Corbett, Handy, & Enns, 2009;Durant & Clifford, 2006;Matin, 1974). Further, neurophysiological results support the finding that neurons are suppressed not only during the presentation of the context (Knierim & van Essen, 1992;Lamme, 1995;Zipser et al, 1996), but up to almost 200 ms after its disappearance (Ishikawa, Shimegi, Kida, & Sato, 2010;Shimegi et al, 2014).…”

“…This strongly manifested and rapidly aroused tilt illusion is supported by data directly recorded from the primary visual cortex of primates and cats. Neuron responses to the CRF stimulus surrounded by an isooriented context start to decrease no more than about 20 ms from the onset of the neuron responses to the CRF stimulus only or to the CRF stimulus with a orthogonally oriented context (Bair, Cavanaugh, & Movshon, 2003;Knierim & van Essen, 1992;Müller, Metha, Krauskopf, & Lennie, 2003;Nothdurft, Gallant, & van Essen, 1999;Shimegi et al, 2014, but see Zipser, Lamme, & Schiller, 1996, who reported a slightly longer onset latency at about 80 ms). Consistently, surround suppression, as indicated by the reduction of evoked magnetic responses in the human visual cortex, is also accompanied with a small response delay (Ohtani, Okamura, Yoshida, Toyama, & Ejima, 2002).…”

Alpha oscillations and traveling waves: Signatures of predictive coding?

“…Several combinations of parameters gave rise to oscillatory IRFs (brighter colors); among these, IRF oscillations in the alpha (8–13 Hz) frequency range were particularly frequent (red colors). In particular, alpha-band IRF oscillations systematically arose when τ and ΔT lay in their “biologically plausible” range of respectively 15–25 ms [15–18] and 10–15 ms [19–21].…”

Dynamics of contextual modulation of perceived shape in human vision

“…With regard to temporal dynamics, most neurophysiological studies have measured the contrast response functions of V1 neurons using luminance gratings drifting at various temporal frequencies, and find strongest suppression of V1 CRF responses from high temporal frequency surrounds 66 67 . Those neurophysiological studies that have examined explicitly the time lag/delay between center and surround responses have used reverse correlation techniques, and find that the suppressive surround effects in V1 neurons peak at around 80 ms after the stimulus onset 68 with the ERF suppression lagging by up to 60–100 ms 41 42 44 68 69 70 71 . For area MT neurons, the inhibitory component of the surround response was found to lag ~10 ms after the center response 72 .…”