Long-range interactions in the lateral geniculate nucleus of the New-World monkey, Callithrix jacchus

Abstract

Visual stimulation of zones extending beyond the classical receptive field can modulate the contrast gain of neurons in the lateral geniculate nucleus (LGN) of cats, but little is known about the effect of extra-classical visual stimulation on the LGN of primates. Hence, we compare the effect of long-range interactions in parvocellular and magnocellular LGN layers of the marmoset monkey Callithrix jacchus using optimal, incremental spots flashed on the classical receptive field either alone or simultaneously with the shift of a grating (98% contrast; 0.1 cycles/deg) confined to a peripheral annulus (radii: 5-15 deg). The contrast required to drive the response halfway to saturation (c50) of most LGN neurons was raised by remote pattern shifts. The c50 ratio [(shift+spot)/spot] in OFF-center magnocellular neurons was significantly higher than in OFF-center parvocellular neurons. OFF-center magnocellular neurons closer to the fovea (<10 deg eccentricity) tended to have a higher c50 ratio than in more peripheral neurons. A significant drop in visual sensitivity to 25% contrast spots was observed during remote motion: d' fell from 1.8 to 1.4 in parvocellular neurons and from 2.2 to 1.7 in magnocellular neurons. Such long-range interactions produce a reduction in visual sensitivity by changing the gain of the geniculate relay and point to an inhibitory, motion-sensitive extra-classical receptive field in both parvocellular and magnocellular pathways, which may be involved in saccadic suppression and attentional mechanisms in early vision.

Linear and Nonlinear Contributions to the Visual Sensitivity of Neurons in Primate Lateral Geniculate Nucleus

“…In large fields, the major effect of the suppressive mechanisms was instead to divide the evoked discharge rate by a constant. This is consistent with previous work in marmoset LGN, which shows that stimuli placed in a region around the classical receptive field will bring about a reduction in response gain (Camp et al 2009;Felisberti and Derrington 2001;Solomon et al 2002;Webb et al 2002). The mechanism that gives rise to the sensitivity reduction that is evident during stimulation with small fields is thus either unresponsive in large fields or its functional signature is overwhelmed by the reduction in response gain; regardless, it is clear that under most visual conditions, responsivity is modulated by multiple suppressive mechanisms with different functional characteristics (Camp et al 2009;Zaghloul et al 2007).…”

Suppressive Surrounds and Contrast Gain in Magnocellular-Pathway Retinal Ganglion Cells of Macaque

“…One argument against a single mechanism underlying all of the effects we describe is that the spatial extent of the ECRF seemed quite different in the two experiments: remote patterns with an inner diameter of 4°were very effective at suppressing probe responses [other studies have shown similar effects for even larger inner diameters Felisberti and Derrington, 2001)], but increasing the diameter of a grating patch from 4 to 8°had little effect on response. If the effectiveness of the ECRF is limited to some maximal value (and thus saturates for strong inputs), expanding the drifting grating may not reveal its full extent.…”

“…More recently, remote moving patterns have been found to cause an increase or decrease in the discharge rate of cat ganglion cells, depending on the spatial and temporal structure of the stimulus (Passaglia et al, 2001). Periphery-effects are generally weaker in primate retinal ganglion cells and LGN cells Felisberti and Derrington, 2001), which is probably related to the general observation that the spatial nonlinearities exhibited by cat Y cells are rarely found in the primate (Hochstein and Shapley, 1976a;Shapley et al, 1981;Blakemore and Vital-Durand, 1986;White et al, 2002). We first show that MC-cell responses to brief probes are generally suppressed by simultaneous changes in surrounding patterns.…”

“…The rest of the field was held at the mean luminance (Felisiberti and Derrington, 1999Derrington, , 2001). Without the surrounding grating, the neuron responded robustly to the probe.…”

The uses of colour vision: behavioural and physiological distinctiveness of colour stimuli

“…(a) Physiological recording Physiological preparation for recording from neurons with microelectrodes and for presenting visual stimuli were essentially as have been described previously (Felisberti & Derrington 2001). …”