Perceptual decision related activity in the parallel pathways of the lateral geniculate nucleus (LGN)

Abstract

Early physiological recordings revealed the exquisite sensitivities of single sensory neurons to subtle changes in stimulus intensity. These observations, however, were reported almost exclusively in anesthetized, paralyzed animals, making it difficult to directly link measured neural sensitivity to the psychophysical sensitivity of the animal. Furthermore, sensory neural responses in cortex are known to covary with the perceptual decisions of the animal in the absence of any external stimulus, but such relationships are never measured in the thalamus. We recorded from different classes of cells in the lateral geniculate nucleus (LGN) of awake monkeys performing two alterative forced choice (2AFC) contrast detection tasks. We found that the majority of single LGN neurons were not as sensitive as the monkeys in detecting contrast, and yet the covariation between LGN neural responses and perceptual choices (quantified as choice probability) was significantly above chance. A bottom-up pooling model that weighted each LGN neuron according to its signal-to-noise ratio (quantified as d-prime) was able to fully explain these observed sensitivity and choice probability data, supporting the hypothesis that in contrast detection the perceptual decision pool consists of multiple thalamic neurons, and that response fluctuations in these neurons can influence contrast perception, with the more sensitive thalamic neurons likely to exert a greater influence. Finally, a detailed comparison between the ON and OFF pathways in contrast increment and decrement detections revealed that OFF neurons responded more robustly and reliably to contrast decrements than ON neurons did to contrast increments, and that the more bursty, fast firing OFF neurons may rely heavily on the visual onset latencies of the first few spikes to relay contrast information.